The Importance of Fossils in Understanding the Evolution of Parasites and Their Vectors

CHAPTER ONE

The Importance of Fossils in Understanding the Evolution of Parasites and Their Vectors Kenneth De Baets*, 1, D. Timothy J. Littlewoodx, 1 *Fachgruppe Pal€aoUmwelt, GeoZentrum Nordbayern, Friedrich-Alexander-Universit€at Erlangen-N€ urnberg, Erlangen, Germany x Department of Life Sciences, Natural History Museum, London, UK 1 Corresponding authors: E-mail: [email protected]; [email protected]

Contents 1. Introduction 2. Techniques for Ancient Parasite Discovery 2.1 Thin sections and computed tomography 2.2 Ancient biomolecules

2 4 5 6

2.2.1 Ancient DNA 2.2.2 Palaeoproteomics

6 7

3. The Parasite Fossil Record 3.1 Body fossils 3.2 Trace fossils and pathologies 3.3 Coprolites 4. Molecular Perspectives on Parasite Phylogeny and Evolution 4.1 Molecular clocks 4.2 HGT and ‘parasitic DNA’ 5. Future Perspectives Acknowledgements References

8 14 18 22 26 29 34 35 36 36

Abstract Knowledge concerning the diversity of parasitism and its reach across our current understanding of the tree of life has benefitted considerably from novel molecular phylogenetic methods. However, the timing of events and the resolution of the nature of the intimate relationships between parasites and their hosts in deep time remain problematic. Despite its vagaries, the fossil record provides the only direct evidence of parasites and parasitism in the fossil record of extant and extinct lineages. Here, we demonstrate the potential of the fossil record and other lines of geological evidence to calibrate the origin and evolution of parasitism by combining different kinds of dating evidence with novel molecular clock methodologies. Other novel methods promise to provide additional evidence for the presence or the life habit of pathogens Advances in Parasitology, Volume 90 ISSN 0065-308X http://dx.doi.org/10.1016/bs.apar.2015.07.001

© 2015 Elsevier Ltd. All rights reserved.

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Kenneth De Baets and D. Timothy J. Littlewood

and their vectors, including the discovery and analysis of ancient DNA and other biomolecules, as well as computed tomographic methods.

1. INTRODUCTION Parasitism is one of the most successful modes of life, as evidenced by its convergent appearance in numerous lineages and its sheer absolute and relative abundance among extant biodiversity (Poulin and Morand, 2000). Antagonistic interactions, in the form of arms races between parasites and their hosts, have been considered important drivers of evolution (Zaman et al., 2014) and might also have contributed to the origin of sexual reproduction (Mostowy and Engelst€adter, 2012). Because parasitism also has an obvious societal importance with many parasitic taxa being of significant biomedical, veterinary or economic importance (Bush et al., 2001), it is here that most of the research effort is focused. This focus is narrow and fails to provide the wider evolutionary picture or an appreciation of the influence of parasitism on, and as part of, biodiversity. Indeed, despite their importance and ubiquity, the evolutionary history of parasites is still poorly known, a phenomenon not helped by their inadequate, or rather inadequately explored, fossil record (Littlewood and Donovan, 2003). Establishing time-calibrated evolutionary frameworks to test the origins and radiations of parasites in parallel with studies on environmental parameters, or the degree of coevolution between parasites and hosts, is a difficult but as yet a largely unexplored means by which ancient associations may be revealed. Parasitologists have often resorted to more circular lines of evidence, such as extrapolating from current host associations or distributions to put time constraints on the origins and evolution of parasites. For instance, where extant hosteparasite associations appear to be combinations of early divergent hosts and early divergent parasites, it is tempting and compelling to assume a long and ancient association; for example, early divergent gyrocotylidean cestodes found only parasitizing early divergent ‘primitive’ holocephalan fishes (Xylander, 2001). In these cases, when the timing of a host’s divergence can be estimated from molecular or preferably fossil evidence, a calibration point for the parasite’s association also appears tractable, at least as a working hypothesis. Assumptions of cophylogeny are common but bring their own suites of problems, not in the least because of the traps set by multiple assumptions (Page, 2003). To reveal coevolutionary patterns, phylogenies of hosts and parasites need to be untangled to better understand

The Importance of Fossils in the Evolution of Parasites

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historical relationships, but the task is complex. Accurate estimates of historical events such as co-divergence, duplication or loss of an association require complex mathematics and computationally demanding algorithms, and any estimate is contingent upon adequate sampling (Charleston and Perkins, 2006). Usually such sampling relies on phylogenies determined from extant organisms and pays little heed to loss of lineages through extinction. Whilst these studies can be profitable, direct evidence from the fossil record remains the most compelling evidence for past historical and deep evolutionary associations, as well as extinctions. Palaeontological data could also have a bearing on testing of how parasiteehost associations respond to environmental changes across longer time-scales and to what extent parasites could be prone to (co)extinction (Dunn et al., 2009). The past decades have seen a wealth of new discoveries, ranging from exceptionally preserved parasites and eggs assignable to modern (even family level) lineages (Cressey and Boxshall, 1989; Da Silva et al., 2014; Hugot et al., 2014), to characteristic traces of preserved biomolecules in host remains (Dittmar, 2009; Greenwalt et al., 2013; Wood et al., 2013b). Of particular note have been advances in X-ray, ion, electron and laser-beam techniques, serial grinding/imaging techniques and magnetic resonance tomography characterizing fine structures, textures and underlying chemistries (Mietchen et al., 2008; Sutton, 2008; Schiffbauer and Xiao, 2011; Dunlop et al., 2012; Cunningham et al., 2014a,b; Sutton et al., 2014). Additionally, advances in mass spectrometry have allowed the detection and characterization of amino acid traces, particularly collagen within bone, to a remarkable level of detail and resolution (Cappellini et al., 2014). Such techniques open up the prospect of detecting traces of parasites and parasitism more frequently and revealing key systematic features and morphological characters indicative of a parasitic way of life. Another facet of palaeoparasitology, although perhaps not widely considered as such, is the study of horizontally (laterally) transferred DNA including transposable elements, where DNA from one organism can be detected buried within the genome of another. These so-called ‘genomic fossils’ offer clues as to the origins and nature of ancient associations (Gilbert and Feschotte, 2010; Gilbert et al., 2010; Katzourakis and Gifford, 2010; Katzourakis, 2013; Koutsovoulos et al., 2014). Indeed, Ford Doolittle considers horizontally transferred DNA fragments as ‘basically parasites’ (p. 8; Gitschier, 2015) that have been parts of their host genomes for a considerable length of time. The rise in genome studies has provided ever-increasing evidence for horizontal gene transfers, HGTs

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Kenneth De Baets and D. Timothy J. Littlewood

(e.g. see Scholl et al., 2003), although such events detected among Metazoa appear to be more common in some groups (e.g. bdelloid rotifers: Gladyshev et al., 2008) than in others. Whereas palaeontology looks towards the earth’s fossil and subfossil record for ancient biotic interactions, it is clear that genomes may also be gleaned for evidence of relictual genetic elements of nonhost (“parasitic”) origin. Regardless of approach, time points gathered directly from fossils or inferred from calibrated phylogenies remain critical in understanding when, where and to some extent how hosteparasite interactions took place and how they might respond in the future; for example, the exchange of genes from parasitic to host plants of the genus Plantago has been shown to be a result of their direct physical contact with one another (Mower et al., 2004). Parasitic plants offer a particularly rich resource for understanding HGT (Davis and Xi, 2015). Morphologically based classifications of parasites have proved challenging due to frequent apparent simplifications, convergence or specializations in their morphology that make homology assessment difficult. However, novel molecular methods, used with caution, may form the basis for more robust phylogenetic assignments of extant and subfossil parasitic remains, and thus more comprehensive understanding of the origin and evolution of parasitism within single lineages (Near, 2002; Lockyer et al., 2003; Littlewood, 2011; Wood et al., 2013b; Hartikainen et al., 2014; Summers and Rouse, 2014; Blaxter and Koutsovoulos, 2015; Littlewood and Waeschenbach, 2015; Okamura and Gruhl, 2015). Here we provide an updated perspective on the merits, further possibilities and frustrations associated with using the fossil record in constraining the origins and evolution of parasitism. We highlight novel methods, which make it possible to more fully exploit information buried in fossil or genomic sequences of their hosts.

2. TECHNIQUES FOR ANCIENT PARASITE DISCOVERY Various destructive methods (thin sections, rehydratation or resedimentation techniques, and grinding tomography) and nondestructive methods (e.g. phase contrast synchrotron or microcomputed tomography, mCT) are particularly relevant to discovering and characterizing the morphology of parasitic remains or host responses in older (fossil) samples. Increasingly these can be supplemented with analyses of ancient

The Importance of Fossils in the Evolution of Parasites

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biomolecules, including ancient DNA (aDNA) in younger (archaeological) samples, or analyses of more resistant biomolecules in older, exceptionally preserved fossil samples (Briggs and Summons, 2014).

2.1 Thin sections and computed tomography Various studies have demonstrated the merit of conventional preparation and imaging methods used for archaeological samples (Araujo et al., 2008; Ara ujo et al., 2015) to provide evidence for helminth eggs or other parasitic remains in fossil coprolites (Poinar and Boucot, 2006; Dentzien-Dias et al., 2013; Da Silva et al., 2014). Such investigations typically rely on thin sectioning and various dissolution/rehydration/resedimentation methods, which destroy the original 3D structure and/or association of the parasites and may lose less-resistant parasite remains (Dufour and Le Bailly, 2013; Wood et al., 2013b; Ara ujo et al., 2015). Computed tomography (Sutton et al., 2014), whereby 3D reconstructions of serially sectioned material are rendered and visualized by computer, is developing rapidly as a means by which high resolution differentiation can be achieved from the fossilized remains of small and even soft-bodied organisms. However, the resolution of parasites and evidence of parasitism often remains a serendipitous by-product of investigating fossil microstructures. One such case has recently revealed the remarkable discovery of a putative fossil pentastomid found in association with its ostracod host entombed for 425 Ma (Siveter et al., 2015). Not only did this discovery reveal the first fossil occurrence of an adult pentastomid but also its host association, which had been the subject of some considerable speculation in the literature (Waloszek et al., 2005). Today, pentastomids mostly parasitize terrestrial vertebrates exclusively as endoparasites, and although extinct representatives have been identified in Cambrian marine sediments at a time before these terrestrial hosts existed, it has been suggested that these forms were parasitic on marine vertebrates (Sanders and Lee, 2010). The new Silurian record by Siveter et al. (2015) not only reveals a new host association but also shows the parasite as ectoparasitic. Unfortunately, because of the destructive nature of the grinding technique, the fossil now exists only as an image. Although many reports for terrestrial parasites or vectors come from amber (Poinar, 2014a), computed tomography has only been rarely used to test such assertions (Dittmar et al., 2011; Dunlop et al., 2012), which have been largely based on microscopic methods. Phase contrast tomography and other tomographic methods are however ideally suited to characterize fossils in three dimensions (even in nontransparent amber) and corroborate

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Kenneth De Baets and D. Timothy J. Littlewood

parasite/vector interpretations as it has been used for phoretic associations (Dunlop et al., 2012; Penney et al., 2012).

2.2 Ancient biomolecules Novel techniques make it possible to identify biomolecules (Greenwalt et al., 2013; Briggs and Summons, 2014; Yao et al., 2014) in ancient remains and samples. The most familiar one is probably aDNA, which has been applied to various parasitic (sub)fossils (Dittmar, 2009; Dittmar et al., 2011; Wood et al., 2013b), although it can only be detected and characterized reliably in exceptionally well-preserved material up to 1 Ma (Hebsgaard et al., 2005; Briggs and Summons, 2014). Large and fragile molecules such as DNA cannot survive fossilization (Briggs and Summons, 2014), but other complex organic structures such as iron-stabilized haem, can survive for longer, at least under certain conditions (Briggs, 2013; Greenwalt et al., 2013; Yao et al., 2014), opening up the prospects for protein-based detection methods (Cappellini et al., 2014). This can be used as an extension to the analysis of gut contents of isolated parasite or vector remains to get an indication of the trophic targets and, therefore, the possible identity of the hosts. Preservation of feather remnants in a louse specimen’s foregut, for example, confirmed its association to a waterbird ectoparasite (Wappler et al., 2004). Advances in chemical analysis at the nanoscale, and as applied to fossils, opens up a whole new world in revealing ancient colours, pigments, microbiomes, and the hidden remnants of soft-bodied organisms (Briggs and Summons, 2014; Bertazzo et al., 2015; Vinther, 2015). A better understanding of taphonomy (Briggs, 2013), as applied to parasitic groups, may provide the tools to improve and apply these techniques in recognizing parasites and their influence on hosts in the fossil record. Certainly there seems room for developing and applying these techniques to subfossil (unmineralized) remains where eggs are found intact without DNA and without clear morphological identity (see also Linseele et al., 2013 and Cano et al., 2014). 2.2.1 Ancient DNA Earlier aDNA studies focused on PCR to amplify specific short gene sequences targeted for particular parasite groups or species from single samples (reviewed in Dittmar, 2009; Dittmar et al., 2011; Dittmar, 2014). Novel approaches (Wood et al., 2013b) focus on the amplification of total DNA of whole samples followed by the application of next generation sequencing

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platforms for shotgun sequencing. Subsequent bioinformatic interrogation of the data for various groups of parasites has been established in the field of metagenomics and environmental samples (Dittmar, 2009; Wood et al., 2013b). In spite of remarkable progress, aDNA techniques will always be constrained by the rapid deterioration of DNA.

2.2.2 Palaeoproteomics DNA is not believed to survive in sufficiently long lengths for sequencing over longer geological timescales (>1 Ma) (Hebsgaard et al., 2005; Briggs and Summons, 2014) and is rarely found well preserved. However, the study of fossilized bone, which has been crudely defined as a composite of collagen (protein) and hydroxyapatite (mineral) (see Hill et al., 2015), has shown that, for vertebrates at least, palaeoproteomics can be a rewarding insight into ancient proteins, providing evidence for phylogenetics and an understanding of bone biochemistry (Wadsworth and Buckley, 2014). Collagen, in particular, has been isolated from vertebrate fossils of considerable age, including an 80 million year (my)-old Campanian hadrosaur, Brachylophosaurus canadensis (Schweitzer et al., 2009) and a 68-my-old Tyrannosaurus rex (Asara et al., 2007); some of these studies have attracted some criticism (Pevzner et al., 2008). The characterization of the constituent peptides of fossil bone proteins, requiring mass spectrometry, suggests that collagen (the most abundant protein) can survive up to 340 ky at 20  C, and the second most abundant protein, osteocalcin, can persist for w45 ky; see Ostrom et al. (2000), Hofreiter et al. (2012) and Collins et al. (2000). There are many other bone proteins that can be isolated and identified depending on the nature of preservation and the age of the fossil (Cappellini et al., 2012), but recent studies focusing on collagen have provided opportunities to push timescales back further in the characterization of ancient biomolecules useful for phylogenetics (Welker et al., 2015). Recently, even putative erythrocyte remains were reported in dinosaur bones (Bertazzo et al., 2015). The application of palaeoproteomics more broadly to parasites or to other fossil remains, in the hope of finding evidence for parasitism, is in its infancy, but analysis of more resistant biomolecules than DNA might make it possible to test other hypotheses associated with parasites or hostrelated biomolecules. Certainly, the prospect of verifying the presence of porphyrins in fossilized haematophagous insects (Greenwalt et al., 2013; Yao et al., 2014) seems a tractable goal.

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Kenneth De Baets and D. Timothy J. Littlewood

3. THE PARASITE FOSSIL RECORD The fossil record of parasites or other pathogens is usually poor because they often reside within their hosts or vectors, may go through some life cycle stages away from their hosts, are small, and lack hard tissues (Conway Morris, 1981; Baumiller and Gahn, 2002; Labandeira, 2002; Littlewood and Donovan, 2003; De Baets et al., 2011). This is particularly true not only for viruses, bacteria and protozoa (Poinar, 2014a), but also for various soft-bodied metazoan parasites such as helminths (Littlewood and Donovan, 2003; De Baets et al., 2015a; Huntley and De Baets, 2015; Poinar, 2015a) or weakly sclerotized arthropods (Cressey and Boxshall, 1989; Castellani et al., 2011; Klompmaker and Boxshall, 2015; Nagler and Haug, 2015). Body fossils of parasites are rare and usually restricted to sites of exceptional fossil preservation (KonservateLagerst€atten), particularly those still associated with the remains of their hosts providing direct evidence of parasitism. Characteristic traces or pathologies in the skeletons of their hosts are more common and can be traced more continuously over longer timescales, but the taxonomic affinity of the culprits is not always easy to disentangle (Donovan, 2015; Huntley and De Baets, 2015; Klompmaker and Boxshall, 2015; Taylor, 2015). The fossil record of parasitism has been reviewed on various occasions (Conway Morris, 1981; Boucot, 1990; Littlewood and Donovan, 2003; Boucot and Poinar, 2010; Dittmar, 2010) with some others focusing particularly on marine parasites (Baumiller and Gahn, 2002; Rouse, 2005a) or terrestrial pathogens (Labandeira, 2002; Poinar, 2014a). The fossil record can also provide direct evidence for presence of parasiteehost associations e some of which might now be extinct, as well as the impact of parasitism on their hosts in the geological past. We will discuss the different sources of fossil evidence, their merits, limitations and associated frustrations. Major important fossil discoveries of metazoan parasites and pathogens distributed by vectors underpinning our understanding of the ancient history of hosteparasite associations are detailed in Table 1. The table reveals considerable diversity of hosts and parasites, and hosteparasite interactions. New finds also highlight the potential of finding evidence in coprolites for parasitic remains in both marine and terrestrial realms, and amber as sources for haematophagous vectors. Fossil pentastomids were long thought to be rare and restricted to the CambrianeOrdovician sites with Orsten preservation, but new discoveries highlight they might be more common than

Table 1 Ancient history of hosteparasite associations Higher taxon Taxon Fossil evidence

Age

Source

Host

References

Environment

Bacteria Spirochaetes Rickettsiales

Palaeoborrelia dominicana Palaeorickettsia protera

Direct: spirochaetelike cells Direct: rickettsial-like cells

Miocene

Amber

Amblyomma sp.

Poinar (2014b)

T

Early Cretaceous

Amber

Cornupalpatum burmanicum

Poinar (2015b)

T

Parabasalia: Trichomonadida Entamoebites antiquus

Indirect: lesions

Cretaceous

Tyrannosaurus rex

Wolff et al. (2009)

T

Direct: cyst

Cretaceous

Skeletal deformation Coprolite

Archosaur (?dinosaur)

Poinar and Boucot (2006)

T

Direct: in amber

CretaceouseMiocene

Amber

Cockroaches

Poinar (2012)

T

Direct: aDNA in coprolite Indirect: oocysts Indirect: oocysts

Holocene

Coprolite

Moas

Wood et al. (2013b)

T

Holocene Pleistocene

Coprolite Coprolite

Deer Ground sloth

Ferreira et al. (1992) Schmidt et al. (1992)

Direct: erythocytes Direct: erythocytes Direct: erythocytes

Miocene Miocene Early Cretaceous

Amber Amber Amber

Culex malariager Enischnomyia stegosoma Proticulicoides sp.

Poinar (2005b) Poinar (2011b) Poinar and Telford (2005)

T T T

Direct: erythocytes

Early Cretaceous

Amber

Leptoconops nosopheris

Poinar (2008a)

T

Direct: erythocytes

Miocene

Amber

Triatoma dominicana

Poinar (2005b)

T

Eukaryota Metamonada Amoebozoa?

Phylum Apicomplexa Gregarinasina Coccidia

Haemospororida

Primigregarina burmanica Cryptosporidium, Eimeriorina Eimeria lobatoi Archeococcidia antiquus; A. nothrotheriopsae Plasmodium dominicana Vetufebrus ovatus Paleohaemoproteus burmacis

Phylum Euglenozoa Trypanosomatida

Palaeotrypanosoma burmanicus Trypanosoma antiquus

(Continued)

Table 1 Ancient history of hosteparasite associationsdcont'd Higher taxon Taxon Fossil evidence Age Palaeoleishmania proterus Paleoleishmania neotropicum

Source

Host

References

Environment

Poinar and Poinar (2004a,b) Poinar (2008b)

T

Direct: erythocytes

Early Cretaceous

Amber

Palaeomyia burmitis

Direct: erythocytes

Miocene

Amber

Lutzomyia adiketis

?

Indirect: exocysts

Jurassic

Skeletal deformation

Crinoids, echinoids

Kabatarina pattersoni

Direct:

Early Cretaceous

Calcareous nodules

Fish

Isopoda

?Bopyridae

Indirect: swellings

?Early Jurassic; Middle JurassiceRecent

Skeletal deformation

Crustacea

Pentastomida

5 genera; 10 species

Direct: phosphatized remains isolated from host

Cambrian eOrdovician; Silurian?

Calcareous nodules

? early chordates; ostracod

Acari

Cornupalpatum burmanicum (Ixodidae) Compluriscutula vetulum (Ixodidae)

Direct: larva stage

Early Cretaceous

Amber

?

Direct: larva stage

Early Cretaceous

Amber

?

T

Phylum Arthropoda Copepoda

Mercier (1936), Radwa nska and Radwa nska (2005), Radwanska and Poirot (2010) Cressey and Patterson (1973), Cressey and Boxshall (1989) Klompmaker et al. (2014), Klompmaker and Boxshall (2015) Waloszek and M€ uller (1994), Waloszek et al. (1994), Waloszek et al. (2005a,b), Castellani et al. (2011), Siveter et al. (2015) Poinar and Brown (2003) Poinar and Buckley (2008)

M

M

M

T

T

Thecostraca

?Ascothoracida

Indirect: borings

Cretaceous

Skeletal deformation Skeletal deformation

Echinoidea

?Ascothoracida

Indirect: borings

Cretaceous

Siphonaptera s.l.

Pseudoculidae

Direct: isolated from host

JurassiceCretaceous

Lacustrine deposits

?pterosaurs, dinosaurs and/or small mammals

Siphonaptera s.s.

Paleopsylla: 4 species

Direct: isolated from host

Eocene

Amber

?mammals

Phthiraptera

Megamenopon rasnitsyni

Eocene

Diptera

? Qiya jurassica (Athericidae)

Direct: isolated from host Indirect: nits Direct: parasitic larvae

Eocene Jurassic

Lacustrine deposits Baltic amber Lacustrine deposits

Indirect: eggs

Upper Triassic

Direct: egg with developing juvenile Direct: eggs Indirect: eggs

Octocorallia

Madsen and Wolff (1965) Voigt (1959), (1967)

M M

Insecta T

?water birds

Gao et al. (2012), Huang et al. (2012), Gao et al. (2013), Huang et al. (2013), Gao et al. (2014), Huang (2014) Dampf (1911), Beaucournu and Wunderlich (2001), Beaucournu (2003) Wappler et al. (2004)

Mammals ?salamanders

Voigt (1952) Chen et al. (2014)

T F

Coprolite

Cynodont

Da Silva et al. (2014)

T

Early Cretaceous

Coprolite

Archosaur

T

Pleistocene

Cave deposits

Upper Triassic

Coprolite

Canid (?Crocuta spelaea) Cynodont

Poinar and Boucot (2006) Bouchet et al. (2003) Hugot et al. (2014)

T

T

F

Phylum Nematoda Ascaridida

Oxyurida

Ascarites rufferi (Ascarididae) Ascarites gerus (Ascarididae) Toxocara canis (Ascarididae) Paleoxyuris cockburni (Heteroxynematidae)

(Continued)

Table 1 Ancient history of hosteparasite associationsdcont'd Higher taxon Taxon Fossil evidence Age

Source

Host

References

Environment

Midge (Chironomidae: Diptera) Early land plant

Poinar et al. (1994)

T

Poinar et al. (2008)

T

Poinar and Buckley (2006)

T

Dentzien-Dias et al. (2013), De Baets et al. (2015a) Poinar and Boucot (2006) Jouy-Avantin et al. (1999) Ruiz and Lindberg (1989), Todd and Harper (2011), Huntley and De Baets (2015) Upeniece (2001, 2011), De Baets et al. (2015a)

M

Mermithida

Cretacimermis libani (Mermithidae)

Direct

Early Cretaceous

Amber

?Enoplida

Palaeonema phyticum (Palaeonematidae)

Direct

Early Devonian

Silicified plant material

Direct

Early Cretaceous

Amber

Permian

Direct: eggs with developing embryo

Coprolite

Sharks

Digenites proterus

Early Cretaceous

Indirect: eggs

Coprolite

Archosaurs

Dicrocoelidae

Pleistocene

Indirect: eggs

Coprolite

?bear

?Gymnophallidae

Early Eocene

Indirect: characteristic pits in bivalve shells

Skeletal deformation

Middle Devonian

Direct: attachment structure

Fine-grained sediments

Phylum Nematomorpha Chordodidae

Cretachordodes burmitis

Phylum Platyhelminthes Cestoda

Trematoda

?Monogenea

Placoderms, acanthodians

T T M

Phylum Acanthocephala ?

?

Holocene

Indirect: eggs

Carboniferous eJurassic Triassic

Indirect: skeletal deformations (galls) Indirect: cocoons

Coprolite

Mammals (canids, humans)

Fry and Hall (1969), Noronha et al. (1994)

T

Crinoids

Welch (1976), Hess (2010) Manum et al. (1991), Bomfleur et al. (2012), Parry et al. (2014)

M

Sohl (1964) Neumann and Wisshak (2009) Dockery (1980)

M M

Phylum Annelida Myzostomida

?

Clitellata

?Hirudinae

Freshwater deposits

?

F

Direct: isolated shells Indirect: trace on echinoid hosts Direct: isolated shells

Marine deposit Skeletal deformation Marine deposit

? Echinoids

OligoceneeMiocene

Direct: shells associated with coral host

Skeletal deformation

Corals (Cladocera, Thegioastraea, Pocillopora)

Lozouet and Renard (1998)

M

Quaternary

Direct: glochidium larvae

Freshwater deposits

?fish

Brodniewicz (1968)

F

Phylum Mollusca Eulimidae

Eulima ?

Upper Cretaceous Upper Cretaceous

Coriaphyllidae

Coralliophila (Timothia) aldrichi Leptoconchus: 2 species; Coralliophila: 1 species; Galeropsis: 1 species Unio, Anodonta

Eocene

Unionidae

?

M

14

Kenneth De Baets and D. Timothy J. Littlewood

expected even during different ages. Such fossil Lagerst€atte should therefore be systematically screened for parasites. Further work needs to be done on establishing characteristic trace fossils and pathologies, particularly in vertebrates, back in time.

3.1 Body fossils Body fossils are usually defined as remains or representations of the whole or actual parts of organisms (Goldring 1999; Foote and Miller, 2007). In rare cases, parasites are so well and completely preserved that they can be accurately assigned to modern taxa (Cressey and Boxshall, 1989; Siveter et al., 2015). Often, only sclerotized attachment organs, eggs or cysts are known, which can still be characterized sufficiently to assign them to particular taxa (De Baets et al., 2015a). In other cases, body fossils of nonparasitic life stages of extant parasites hint that their parasitic life stages might potentially also be present (e.g. parasitic stages of arthropods or unionids), but this can only be confirmed by future discoveries (Skawina and Dzik, 2011; Nagler and Haug, 2015). All extant members of Unionida have parasitic larvae, which suggests that this is a synapomorphic trait for this group, which goes as far back as the middle Triassic (Skawina and Dzik, 2011). Unfortunately, the oldest fossil glochidia cannot be used to test this hypothesis as they are only found as late as the Pleistocene (Brodniewicz, 1968). In exceptional cases, parasite body fossils are still associated with host remains, while in other cases they are isolated, making it difficult to identify the hosts or even decide if these forms were parasitic or not. Establishing them as parasites is usually achieved by comparing them with the morphology of modern relatives or analogues, but in some cases it can only be corroborated by finding the parasite in situ parasitizing its host. Labandeira (2002), for example, claims that Cambrian tardigrades (Muller et al., 1995) have certain resemblances to extant parasitic forms, which indicates at least a possible phylogenetic relationship and potentially a mode of life, but this still needs to be further corroborated. The body fossil record is restricted to sites of exceptional preservation. One of the most important types of preservation is found in fossil ambers which have preserved the remains of unicellular pathogens from a variety of terrestrial parasitic arthropods (Nagler and Haug, 2015), to nematodes exiting their dying hosts (Poinar, 2014a, 2015a). Other important Konservat Lagerst€atten for the preservation of parasites include phosphatized remains of arthropods (Cressey and Patterson, 1973; Cressey and Boxshall, 1989; Maas and Waloszek, 2001; Maas et al., 2006) in carbonate nodules (the so-called Orsten preservation), silicified nematodes (Poinar et al., 2008) in

The Importance of Fossils in the Evolution of Parasites

15

hydrothermal vent environments (the so-called Rhynie Chert preservation), fine-grained lacustrine or marine deposits where the remains were quickly buried and/or anoxic environments contributed to fossilization. The latter includes oil shales deposited not only in maars or other lacustrine environments (Wappler et al., 2004; Hughes et al., 2010; Greenwalt et al., 2013), but also in low energetic, marginal marine or deeper marine environments. In some cases, ectoparasites are still attached or associated with their hosts, while endoparasites are still found in situ within their hosts or escaping their dead hosts. Cysts, eggs including those with developing embryos, larvae (Ferreira et al., 1993) or remains of juveniles, are sometimes also recovered from coprolites, one of the many types of trace fossils (see Section 3.2). Protozoan parasites or other pathogens like viruses and bacteria are usually hard to verify in the fossil record (Frías et al., 2013; Poinar, 2014a), but are known to be transmitted by various vectors, which might themselves fossilize. Most common vectors are arthropods which feed on blood, although forms feeding on feathers or hairs might also be involved. Direct fossil evidence for vector feeding behaviour is even rarer than parasitism (Table 2). Possible exceptions include the recent discovery of haemoglobin-derived porphyrins in the stomach content of an Eocene mosquito (Greenwalt et al., 2013) as well as higher Fe contents in fossilized true bugs, Hemiptera (Yao et al., 2014). Direct evidence for vector behaviour of haematophagous taxa has been restricted so far to amber deposits (Poinar and Poinar, 2004b; Poinar, 2005a,b,c; Poinar and Telford, 2005; Poinar, 2011b, 2014b, 2015b). Some unicellular pathogens have also been reported from fossil and subfossil archosaur coprolites, although microscopic taxa are harder to identify in older occurrences than in more recent occurrences where aDNA is available (Poinar and Boucot, 2006; Wood et al., 2013b). Our ability to identify parasitic and haematophagous insects is mostly based on their possible taxonomic affinities and morphological adaptions of their mouth parts or other structures similar to extant taxa (Lukashevich and Mostovski, 2003; Greenwalt et al., 2013; Pe~ nalver and Pérez-De la Fuente, 2014; Nagler and Haug, 2015). Such morphological adaptations have even been used to suggest ectoparasitic behaviour in lineages where larvae are no longer parasitic (Chen et al., 2014). Modern-type lice can be traced back to the Eocene (Wappler et al., 2004), while earlier reports are most likely erroneous determinations of mites (Dalgleish et al., 2006), so that Phthiraptera, which are mainly specialized on mammals, probably evolved later than did fleas (Nagler and Haug, 2015). Fossils of modern-type fleas can be traced back to the Eocene at least

16

Table 2 Body fossils of haematophagous vectors Taxonomy Species Haematophagy

Parasite

Source

References

Arachnida Cornupalpatum burmanicum Amblyomma sp.

Indirect Indirect

Rickettsial-like cells Spirochaete-like cells

Burmese amber Dominican amber

Poinar (2015b) Poinar (2014b)

Ceratopogonidae

Proticulicoides sp.

Indirect

Plasmodiidae

Burmese amber

Culicidae

Leptoconops nosopheris Culiseta sp.

Trypanosomatidae ?

Burmese amber Kishenehn Formation

Culex malariager Palaeomyia burmitis Lutzomyia adiketis Enischnomyia stegosoma

Indirect Direct Fe concentrations, porphyrins Indirect Indirect Indirect Indirect

Poinar and Telford (2005), Boucot and Poinar (2010) Poinar (2008a) Greenwalt et al. (2013)

Plasmodiidae Trypanosomatidae Trypanosomatidae Plasmodiidae

Dominican amber Burmese amber Dominican amber Dominican amber

Poinar (2005a,b) Poinar and Poinar (2004a,b) Poinar (2008b) Poinar (2011b), Poinar and Brown (2012)

Triatoma dominicana Torirostratus pilosus Flexicorpus acutirostratus

Indirect Direct Fe concentrations Direct Fe concentrations

Trypanosomatidae ? ?

Dominicsssan amber Yixian Formation Yixian Formation

Poinar (2005c) Yao et al. (2014) Yao et al. (2014)

Ixodidae

Diptera

Streblidae

Hemiptera Reduviidae Torirostratidae Torirostratidae

Kenneth De Baets and D. Timothy J. Littlewood

Phlebotomidae

The Importance of Fossils in the Evolution of Parasites

17

(Perrichot et al., 2012), although several extinct families of putative stemgroup Siphonaptera have been reported from the Jurassic and Cretaceous periods (Gao et al., 2012, 2013, 2014; Huang et al., 2012, 2013; Huang, 2014, 2015). Host associations with dinosaurs and pterosaurs have been suggested for stem-group fleas (Huang, 2014), but a novel molecular study suggests that the earliest fleas appeared in the early Cretaceous era and had a strong association with mammals, whereas the Jurassic stem-group forms are only distantly related (Zhu et al., 2015). Finding direct evidence of Jurassic or Cretaceous fleas associated with host remains would be the smoking gun to resolve this issue. The relationship between hosts and other haematophagous insects, which are also important vectors, is less strict. Bed bugs and their close relatives can probably be traced back to the Eocene (Engel, 2008). Diptera can be traced back to the PermianeTriassic. Blood-sucking is inferred to be ancestral in this group and members of various lineages are important vectors (Poinar, 2014a; Nagler and Haug, 2015), including blackflies (Simulidae), sandflies (Phlebotominae, Psychodidae) and mosquitoes (Culicidae). Direct evidence for both haematophagy and their vectors is only known from Diptera (Greenwalt et al., 2013; compare Table 2). Ticks are also important vectors for Spirochaetes and Ricketsiales, which might have been already the case since the Cretaceous period (Poinar, 2014b, 2015b). Even when isolated from their hosts, gut contents or coprolites of fossil parasitic invertebrates (Wappler et al., 2004; Greenwalt et al., 2013) or vertebrate hosts (McConnell and Zavada, 2013), as well as other remains found alongside, have allowed parasite remains to be confidently attributed to major host groups, at least at higher taxonomic levels (Dentzien-Dias et al., 2013; Da Silva et al., 2014; Hugot et al., 2014). Archaeological examples frequently allow species level identifications of helminth eggs (Dittmar et al., 2011). The earliest evidence for Metazoa parasitizing a plant is nematodes found within early land plants (Poinar et al., 2008). Nevertheless, fungi can also be vicious pathogens of animals and plants (Sexton and Howlett, 2006). The oldest evidence for the presence of fungi parasitic on animals derives from the Cretaceous period (Sung et al., 2008). Sometimes, the characteristic response of the host to a fungal parasite can also be preserved (see Section 4.2). Fossilized galls can also be important sources of information on planteparasite interactions (Knor et al., 2013; Labandeira and Currano, 2013; Leckey and Smith, 2015). Note that galls are often caused by parasitic insects, but can also be induced by viruses, bacteria, fungi, nematodes and mites (Knor et al., 2013).

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Kenneth De Baets and D. Timothy J. Littlewood

3.2 Trace fossils and pathologies Various invertebrate hosts including arthropods, molluscs, echinoderms and various colonial organisms can contain traces or pathologies in their skeleton, which is evidence of an infestation or association with parasites (Boucot and Poinar, 2010; Donovan, 2015; Huntley and De Baets, 2015; Taylor, 2015). In some cases, these traces or pathologies are believed to be so characteristic that they are interpreted to represent the oldest fossil evidence for particular lineages in the fossil record; including castration of fossil decapods by rhizocephalan barnacles (Feldmann, 1998, 2003; compare Klompmaker and Boxshall, 2015), deformations in echinoderms attributed to myzostomid annelids (Welch, 1976; Hess, 2010; Parry et al., 2014), crustacean arthropods (Madsen and Wolff, 1965; Radwa nska and Radwa nska, 2005; Radwanska and Poirot, 2010) or eulimid gastropods (Neumann and Wisshak, 2009) as well as borings in octocorals related to the presence of ascothoracid barnacles (Voigt, 1959, 1967). The most convincing palaeontological model systems are those where both extant and fossil parasiteehost interactions are comparably well studied such as the gymnophallid-induced pits and igloo-shaped shell concretions in bivalves (Campbell, 1985; Ruiz and Lindberg, 1989; Ituarte et al., 2001, 2005; Huntley, 2007; Todd and Harper, 2011; De Baets et al., 2015a; Huntley and De Baets, 2015) and (?bopyrid) isopod swellings in decapods (Weinberg Rasmussen et al., 2008; Boyko and Williams, 2009; Williams and Boyko, 2012; Klompmaker et al., 2014; Klompmaker and Boxshall, 2015). Particularly in such cases, trace fossils and associated pathologies can not only provide direct information on the behaviour of the parasites but also the response of the host, which makes it possible to interpret the type of relationship between them. However, even in the case of such model systems, it cannot be ruled out that they were made by another type of closely related parasite or organism with similar behaviour in the geological past, which are now extinct or where pathological reactions are not yet documented in extant hosts. Other (now extinct) culprits can be suspected when the record of these structures is not so continuous and shows major stratigraphic gaps (Boucot and Poinar, 2010). For example: shell pits have been confidently linked with gymnophallid flatworms in extant bivalves, and can be confidently traced into the Eocene (Ruiz and Lindberg, 1989; Todd and Harper, 2011; De Baets et al., 2015a; Huntley and De Baets, 2015), which is more or less consistent with the origin of their final hosts (extant shorebirds). However, igloo-shaped concretions e attributed to

The Importance of Fossils in the Evolution of Parasites

19

gymnophallids in extant bivalves (Ituarte et al., 2001, 2005), have also been reported from the Silurian (Liljedahl, 1985), which is not consistent with extant parasiteehost associations (De Baets et al., 2015a) as shorebirds (Charadriiformes), their present day definitive hosts, are believed to have radiated sometime between the Cretaceous and Eocene periods (Smith, 2015). Pathologies, therefore, offer less confident evidence for the presence of parasitic lineages in the fossil record than in body fossils, when no parasitic remains are found associated with these traces. Direct evidence for the parasites associated with such pathologies is mostly restricted to parasitic organisms with mineralized skeletons such as gastropods (Hayami and Kanie, 1980; Lozouet and Renard, 1998; Baumiller and Gahn, 2002). Such traces are usually compared with known responses to parasites by extant hosts, which are sometimes not that well-investigated, and by extrapolation it has been assumed that the same culprits were responsible in the past. This can be further complicated by the fact that extant phylogenies indicate that pathology-inducing lineages might have evolved more than once (e.g. gall- and cyst-forming myzostomids: Summers and Rouse, 2014). Parasite-induced pathologies have also been reported from hosts that are now extinct or no longer affected; although their interpretation becomes more difficult if no modern analogues are available (Owen, 1985; Babcock, 2007; De Baets et al., 2011; De Baets et al., 2015b). Traces which are reminiscent of nematode borings in foraminifer tests (Sliter, 1971) have been reported from Cambrian and Ordovician trilobites (Babcock, 2007), but no conclusive assignment to nematodes as culprits can be made without direct fossil evidence for associated nematodes. Furthermore, it is still debated whether these traces in trilobites were made during life or postmortem (Owen, 1985). Various pathological reactions in ammonoids (an extinct group of externally shelled cephalopods) have been attributed to parasitic flatworms based on their prevalence and similar pathologies in extant shelled molluscs (De Baets et al., 2011), but as long as no parasite remains are found associated with them, their attribution to parasitic flatworms remains highly speculative at best (De Baets et al., 2015b). Many palaeontologists also point out the difficulty of defining an interaction as being parasitic, although this might be more a problem concerning the definition of parasitism rather than its recognition (Tapanila, 2008; Zapalski, 2011), which is not restricted to fossil associations. Some authors like Tapanila (2008) have suggested that fossil studies should assume that a symbiosis is neutral (commensal), unless demonstrated otherwise. Other authors have argued that a neutral interaction is absence of an interaction,

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Kenneth De Baets and D. Timothy J. Littlewood

which cannot be proven, and is therefore unfit for empirical science. The detection of commensalism is difficult and rather subjective in recent associations (usually it is understood as a weak positive or negative interaction) and as such it seems impossible to detect in the fossil record. Zapalski (2011) has, therefore, argued avoiding commensalism as a null hypothesis in palaeoecology, because the possibility of making a type II error is very high. Positive or negative effects can be detected or inferred based on comparisons with extant interactions. Identifying traces or pathologies of fossil parasites can potentially also be performed by demonstrating a negative influence or effect on growth, body size and/or morphology of their hosts, while a certain positive effect for the parasite can be inferred. Of course, such interpretations rely on identifying the traces (e.g. borings) or structures as being made in vivo. This can be most convincingly demonstrated when a host response (e.g. growth deformation or pathology) can be shown to be associated with these structures, often most readily recognized in specimens with sparse traces or pathologies (De Baets et al., 2011; Donovan, 2015). Studies have focused particularly on invertebrate hosts, and especially on those with external shells or exoskeletons, but such pathologies which could potentially be tracked in the fossil record are also found in vertebrates including characteristic limb malformations in amphibians (Johnson et al., 2001, 2002, 2003; Johnson and Sutherland, 2003) or cavities in the mastoid bone of humans (Oyediran et al., 1975) caused by digenetic trematodes or trabecula-like bone lesions in cetacean whales (Littlewood and Donovan, 2003) and enlargement of the frontal sinuses accompanied by bone lesions in mustelids (Rothschild and Martin, 2006) caused by cestodes. Characteristic skeletal pathologies in terrestrial vertebrates (e.g. mammals) induced by helminths with resistant eggs have the potential for comparison of prevalence of skeletal deformations directly with parasite load or prevalence in coprolites effectively linking palaeoparasitology and palaeopathology (compare Dutour, 2013). Some parasitic unicellular pathogens might leave characteristic traces or pathologies in their hosts. Wolff et al. (2009) studied erosive lesions in tyrannosaurs and attributed them to Trichomonas gallinaelike protozoans, because they are reminiscent of similar pathologies in extant birds caused by this parasite. Unicellular eukaryotes can also leave characteristic traces in their hosts; for example, borings by foraminifera in marine echinoderms and bivalves (Neumann and Wisshak, 2006; Beuck et al., 2007, 2008). In some cases, the host performs activities or exhibits behaviour induced by the parasites, which can occasionally also be found in the fossil record. One spectacular example is the death-grip scars found on Eocene

The Importance of Fossils in the Evolution of Parasites

21

leaves, interpreted to have been made by ‘zombie’ ants infested by fungi (Hughes et al., 2010); the fungal infection Ophiocordyceps forces ants to hold onto tips of leaves so that after the death of the ant, emerging fungal spores can be released into the wind from an elevated position. Trace fossils can give unique information on the behaviour and prevalence of the parasites and track the response of their host through geological time, as their record can be more continuous (less patchy) than that of body fossils which only fossilize in exceptional conditions. Pathologies have their own problems as they are sometimes hard to assign to a certain lineage of culprits, although there are some pathologies which are believed to be diagnostic, or at least characteristic, for parasitism. Irrespective of this problem, the temporal and spatial record of parasiteinduced pathologies in their hosts can be much more continuous than the parasite body fossil record, particularly in molluscs, echinoderms, colonial organisms and others with fossilizable skeletons (Donovan, 2015; Huntley and De Baets, 2015; Klompmaker and Boxshall, 2015; Taylor, 2015). This can provide valuable quantitative data on various aspects of parasitee host interactions, which can be tracked over millions of years (Brett, 1978; Ruiz and Lindberg, 1989; Baumiller and Gahn, 2002; De Baets et al., 2011; Klompmaker et al., 2014; De Baets et al., 2015b; Huntley and De Baets, 2015; Klompmaker and Boxshall, 2015). Such data can only rarely be obtained by looking at body fossil records of parasiteehost associations, with some rare exceptions where both the host and the parasite have fossilizable skeletons (Lozouet and Renard, 1998; Baumiller and Gahn, 2002) or where multiple similar taphonomic windows (e.g. amber) exist. This includes direct information concerning prevalence and virulence of this relationship, and their possible relationship with host evolution including diversity (Klompmaker et al., 2014) and body size (Ruiz, 1991; Huntley and De Baets, 2015), as well as environmental factors such as sea-level and climate change (Huntley et al., 2014). This can be particularly relevant to predict the future response of parasiteehost systems to global change, where studies have suggested that parasites might be more prone to (co)extinction (Dunn et al., 2009). The link between the prevalence of parasites and pathologies, within populations and particularly individual hosts, might not be straightforward and has only rarely been investigated in extant hosts. Furthermore, the nature of the relationship and their effects might be context dependent (Bronstein, 1994; Daskin and Alford, 2012). Various preservation, collection and taxonomic biases can and should be accounted for in quantitative analyses of fossil

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Kenneth De Baets and D. Timothy J. Littlewood

antagonistic interactions (Huntley and De Baets, 2015; Klompmaker and Boxshall, 2015), which have so far mainly focused on less specific (predatoreprey) interactions (Kelley et al., 2003; Huntley and Kowalewski, 2007) rather than parasiteehost interactions. Various environmental factors can, for example, influence the invasion of molluscs by parasites on various organizational levels (Cheng and Combes, 1990). To further progress in the field of quantitative palaeopathology in deep time, more quantitative data and analyses on existing model systems are required, as well as the need to identify additional modern and/or fossil analogues of already identified parasite-related pathologies. Palaeopathologies with a more continuous fossil record have the potential to be used to model the influence of parasite prevalence and virulence on the evolution of their hosts and how they are modulated by environmental parameters on longer time-scales.

3.3 Coprolites Coprolites are usually defined as fossilized (permineralized) faeces, although the term is often also used for desiccated, more recent faeces from archaeological sites (Ferreira et al., 1991; Reinhard and Bryant, 1992; Hunt et al., 2012). Coprolites have yielded fossil and archaeological evidence for parasitic organisms (Table 3) ranging from coccidia or other protozoans (Ferreira et al., 1992; Schmidt et al., 1992; Poinar and Boucot, 2006; Frías et al., 2013; Wood et al., 2013b), to parasitic fungi and plant remains (Sharma et al., 2005; Wood et al., 2012), to helminths (Gonçalves et al., 2003; Savinetsky and Khrustalev, 2013), including acanthocephalans (Noronha et al., 1994), but particularly nematodes (Ferreira et al., 1991, 1993; Poinar and Boucot, 2006; Leles et al., 2010; Da Silva et al., 2014; Hugot et al., 2014) and various groups of parasitic flatworms (Schmidt et al., 1992; Jouy-Avantin et al., 1999; Dentzien-Dias et al., 2013). Coprolites can therefore be an important additional source of ancient parasitism supplementary to amber, where the record is heavily biased towards arthropods and their terrestrial parasites. In ideal cases, coprolites are still associated with their producer, which makes it possible to confidently identify their origin and therefore the host taxon of the fossil parasites. The coprolite producer may correspond with the host of the parasite or more rarely as the one who ingested the parasite and/or host. However, most frequently, coprolites are found in isolation, where the identity of the producer can only be inferred from their morphology and content (Poinar and Boucot, 2006; Dentzien-Dias et al., 2013), and, in the case of more recent specimens, by aDNA analysis (Wood and Wilmshurst, 2014). Invertebrate coprolites might also have

References

Protozoa Coccidia

Eimeriorina

Oocyst

Holocene

Ground sloth (Nothrotheriops shastensis) Deer Moas (Dinomis robustus, Pachyornis elephantopus)

Schmidt et al. (1992)

Eimeridae Cryptosporidiidae

Oocysts (Eimera) aDNA (Cryptosporidium)

Holocene Holocene

Egg þ developing embryo Eggs Eggs Schistosome-like eggs

Permian

?elasmobranchs

Dentzien-Dias et al. (2013)

Cretaceous Pleistocene Holocene

Archosaur (?dinosaur) Mammal (?bear) Ground sloth (Nothrotheriops shastensis)

Poinar and Boucot (2006) Jouy-Avantin et al. (1999) Schmidt et al. (1992)

Larvae Eggs Eggs

Pleistocene Triassic Triassic

Hyenid Cynodont Cynodont

Ferreira et al. (1993) Da Silva et al. (2014) Hugot et al. (2014)

Ferreira et al. (1992) Wood et al. (2013b)

Helminths Platyhelminthes

Cestoda Trematoda Dicrocoelidae Schistosomatidae

The Importance of Fossils in the Evolution of Parasites

Table 3 Coprolites depicting fossil and archaeological evidence for parasitic organisms Taxonomic affinity Fossil evidence Age Host

Nematoda

? Ascaridomorpha Oxyurida

23

(Continued)

Ascaridomorpha Heterakoidea

Trichocephalida Acanthocephala ?

24

Table 3 Coprolites depicting fossil and archaeological evidence for parasitic organismsdcont'd Taxonomic affinity Fossil evidence Age Host

References

Egg þ developing larvae aDNA

Cretaceous

Archosaur (?dinosaur)

Poinar and Boucot (2006)

Holocene

Wood et al. (2013b)

Eggs (Trichuris)

Pleistocene

Archosaur (Anomalopteryx, Dinornis, Pachyornis, Megalapteryx) Hyenid

Eggs Eggs (Echinopardalis)

Holocene Holocene

Humans Felidae

Fry and Hall (1969) Noronha et al. (1994)

Body remains Body remains

Holocene Holocene

Humans Humans

Johnson et al. (2008) Fry (1977)

Spores

Cretaceous

Archosaur (?dinosaur)

Sharma et al. (2005)

Pollen (Dactylanthus taylorii)

Holocene

Kakapo (Strigops habroptilus)

Wood et al. (2012)

Ferreira et al. (1991)

Arthropods

Fungi

Plant-parasitic fungi Plants

Root-parasite

Kenneth De Baets and D. Timothy J. Littlewood

Ticks Lice

The Importance of Fossils in the Evolution of Parasites

25

the potential to reveal past parasite infections, as demonstrated by reports of a putative trypanosome from faecal droplets found in association with a fossil triatomine in Dominican amber (Poinar, 2005c). Protozoa remains have also been reported from the abdominal region of Miocene Tapir remains (McConnell and Zavada, 2013) as well as in termites preserved in amber (Poinar, 2009). Egg remains are usually considered trace fossils, but they can occasionally contain remains of developing embryos (Poinar and Boucot, 2006; Dentzien-Dias et al., 2013), which are body fossils. Interestingly, parasite eggs have often been found in coprolites or fossilized faeces, which are trace fossils themselves. Some of these coprolites range back to the Palaeozoic (Zangerl and Case, 1976; Dentzien-Dias et al., 2013) or Mesozoic periods (Poinar and Boucot, 2006; Da Silva et al., 2014; Hugot et al., 2014), although most are known from the Cenozoic, particularly the Quaternary era (Ferreira et al., 1991; Jouy-Avantin et al., 1999; Gonçalves et al., 2003). As some of these eggs can be quite resistant to decay, they can also be found in Quaternary sediments, particularly in archaeological sites (Bouchet et al., 2003; Gonçalves et al., 2003; Ara ujo et al., 2015). In other cases, parasite eggs have been reported associated with Cretaceous fossil feathers (Martill and Davis, 1998) or Eocene mammal hair in Baltic amber (Voigt, 1952; Nagler and Haug, 2015). Remains of fossil parasites have typically been revealed through destructive preparation (e.g. thin sectioning, dissolution/rehydration methods) and classical imaging methods leaving little chance for further study, or have been missed or destroyed because of techniques designed to reveal structures of the hosts to which they are associated. Traditional methods of parasite recovery from coprolites, or other ancient samples, can be combined with aDNA techniques (Wood et al., 2013b; Ara ujo et al., 2015) or computed tomography. Sequencing of aDNA might successfully detect very small and/or fragile parasites that may not preserve intact in coprolites, or can be destroyed during the extraction or preparation methods. This method is however also destructive (e.g. samples need to be rehydrated to extract DNA) and restricted to younger (archaeological) samples due to the rapid deterioration of DNA/RNA, making computer tomography particularly important to identify parasites for older (fossil) samples. Tomographic methods might help to reveal additional details of fossils trapped in amber as well as help to discover parasites in coprolites or other ancient remains which can be destroyed during the traditional destructive

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Kenneth De Baets and D. Timothy J. Littlewood

preparation processes. The potential of these windows into parasite evolution has become clear in the last two decades by multiple new discoveries, particularly in marine and terrestrial coprolites (Table 3) as well as in amber fossils (Tables 1, 2). Parasitic remains in fossil coprolites have been reported for a long time (Zangerl and Case, 1976), but were usually received with a certain degree of scepticism (Boucot, 1990; Poinar, 2003). Various methods can yield high-resolution reconstructions of microscopic remains or structures in larger fossils including mCT-scanning or phase-contrast synchrotron tomography (Donoghue et al., 2006; Sutton et al., 2014), but their usefulness depends on the contrast between the fossils and the matrix. Computed tomography can not only be relevant to identify and characterize parasite remains, perhaps to place them in extant phylogenies (Faulwetter et al., 2013; Garwood and Dunlop, 2014), but also to quantify their original position, 3D structure and morphology or association in coprolites or other ancient remains (Dunlop et al., 2012; Siveter et al., 2015). It could potentially be used to study the presence of developing embryos (Donoghue and Dong, 2005; Donoghue et al., 2006; Duan et al., 2012), which have been suggested to be present in some fossil eggs attributed to helminths based on traditional imaging methods (Poinar and Boucot, 2006; Dentzien-Dias et al., 2013). These could even provide supplementary information on the morphology and content of the coprolites, which could make it possible to more confidently identify their host, the coprolite producers, as well as give indications about possible predatoreprey relationships and parasite load. In archaeological studies, coprolites can be quantitatively studied to establish changes in biogeographic distributions and habits of their hosts (Ara ujo et al., 2015; Mitchell, 2015) as well as on parasite body size changes (Fugassa et al., 2008). Additional data are required to quantitatively study these aspects on longer (palaeontological) timescales as the parasitological coprolite studies are still quite patchy in space and time.

4. MOLECULAR PERSPECTIVES ON PARASITE PHYLOGENY AND EVOLUTION Historically, for many taxonomic groups of parasites, morphologically based systematic schemes and phylogenies have been difficult to resolve even in the light of additional sampling or analysis. Parasites often demonstrate high degrees of specialization compared with their free-living relatives, high degrees of reduction or apparent simplification, specialization and/or convergence in morphology related to their parasitic lifestyle. Complex life cycles

The Importance of Fossils in the Evolution of Parasites

27

involving multiple hosts or even a single host can consist of morphologically distinct ontogenetic stages making homology assessment and the identification of shared features even more difficult (Brooks and McLennan, 1993). Molecular methods have the potential to resolve many problems where morphology has been problematic, as long as one can properly deal with biases and spurious signal related to long-branch attraction, sampling, (host) contamination and other issues arising from a purely molecular approach (Edgecombe et al., 2011). Contamination is not only relevant for aDNA (Shapiro and Hofreiter, 2014), but might also be responsible for wrong assignment of various groups of extant parasites. Previously erroneous assignment of Myxozoa, including the vermiform Buddenbrockia, with other taxa has been attributed to host contamination (Jiménez-Guri et al., 2007). On the other hand, molecular studies have had a considerable impact on the assignment of some parasite groups within the broader context of metazoan evolution (Zrzavý, 2001; Edgecombe et al., 2011). For example, pentastomids, long considered to be a separate phylum, are now considered to be closely related to fish lice based on molecular evidence (Sanders and Lee, 2010; Oakley et al., 2012). Also, Myxozoa are now considered to be cnidarians based on molecular evidence (Jiménez-Guri et al., 2007; Hartikainen et al., 2014; Okamura and Gruhl, 2015; Okamura et al., 2015). The phylogenetic position of myzostomids has also been long debated, but most authors now agree that they belong within the Annelida based on molecular analyses (Parry et al., 2014; Summers and Rouse, 2014). The discovery of Chromera velia, the first photosynthetic apicomplexan with a fully functional plastid, might also provide a powerful model to study the evolution of parasitism in Apicomplexa. Molecular analyses indicate that it is the closest relative to apicomplexan parasites, indicating that the plastid of this coral symbiont shares its origin with the apicoplasts (Moore et al., 2008; Okamoto and McFadden, 2008). Acanthocephala (thorny-headed worms) were occasionally compared to priapulids (penis worms) based on morphological evidence (Conway Morris and Crompton, 1982), but are now aligned with Rotifera within the Syndermata (Weber et al., 2013; Wey-Fabrizius et al., 2013). Most recent molecular studies with greater coverage indicate a particular route to parasitism within Platyhelminthes and a closer relationship between cestodes and trematodes (Lockyer et al., 2003; De Baets et al., 2015a; Egger et al., 2015; see Littlewood and Waeschenbach, 2015 for a review), although there are some exceptions (Laumer et al., 2015), which illustrate that the relative importance of particular gene regions needed to disentangle phylogenetic

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Kenneth De Baets and D. Timothy J. Littlewood

relationships still need to be better understood. A recent molecular study (Struck et al., 2014) also indicates that the Platyzoa, which groups Acanthocephala and Platyhelminthes among various free-living taxa, is probably an artefact of long-branch attraction, whereby distantly related lineages are incorrectly inferred to be closely related because both lineages have undergone a considerable amount of change. This theory has since been confirmed by Egger et al. (2015), who demonstrated that only the fastevolving quartile of their transcriptomic dataset supported the Platyzoa. Importantly, in the absence of phylogenetic artifacts, molecular studies can be used to investigate the origins and radiations of parasitic lineages. This has been shown for acanthocephalans (Near, 2002; Wey-Fabrizius et al., 2014), parasitic flatworms (Lockyer et al., 2003), myzostomid annelids (Summers and Rouse, 2014) and nematodes (Dorris et al., 1999; Blaxter, 2003; Blaxter and Koutsovoulos, 2015). Sister-group relationships within and between parasite lineages, the determination of free-living sister groups and the inference of ancestral life history strategies are key to determine the origins of parasitism and the evolution of complex life cycles. The evolution of complex life cycles is a major research question, with two main mechanisms proposed (Parker et al., 2015): upward incorporation by terminal addition of hosts, or downward incorporation by addition of intermediate hosts. Cladistic studies, or the application of parsimony principles to infer ancestral life cycles, have yielded some controversial hypotheses as to the origins and development of ontogenetic sequences (O’Grady, 1985). In parasitic flatworms (Neodermata), complex parasite life cycles appear to have initially evolved by the addition of intermediate hosts, with vertebrate definitive hosts argued to be the plesiomorphic condition for stem group neodermatans (Littlewood et al., 1999); the scenarios are inferred from molecular phylogenies of extant taxa; however, fossil vertebrates may yet hold the key to verifying or at least supporting this claim. Since their initial application, molecular clock methodologies have undergone major developments (Bromham and Penny, 2003; W€ orheide et al., 2015), with ever more sophisticated models accommodating large genomic datasets, rate variation and the uncertainties of multiple types of calibration points (Parham et al., 2012; Ho, 2014). Nevertheless, molecular clocks still need age constraints from the fossil record or other lines of evidence to provide calibration points for at least one or more nodes in a calibrated phylogeny (Ho and Phillips, 2009; Hipsley and M€ uller, 2014; Warnock, 2014). The use of fossils in molecular clocks has changed in the last decades (Parham et al., 2012; Ho, 2014; W€ orheide et al., 2015)

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including their implementation as probabilistic time priors (Ho and Phillips, 2009; Warnock et al., 2015) and tip calibrations integrated among their living relatives by combing molecular and morphological evidence (Pyron, 2011; Ronquist et al., 2012; Wood et al., 2013a; Arcila et al., 2015). However, methods using other types of age evidence like geological calibrations (e.g. vicariance events) or host calibrations lag behind in their development and leave them heavily scrutinized (Goswami and Upchurch, 2010; Kodandaramaiah, 2011; Hipsley and M€ uller, 2014). Finally, advances in molecular techniques have provided additional advances in unravelling past events. aDNA techniques have made it possible to obtain pathogen DNA from dated ancient parasites or host remains (Dittmar, 2009; Bos et al., 2015; Hofreiter et al., 2015). Although many of these studies have been targeted in their approach, there are also those that have characterized complete biomes (Rawlence et al., 2014); for example, detection and characterization of bacteria entombed in dental calculus (Warinner et al., 2015), and the discovery of subfossil coprolites (Santiago-Rodriguez et al., 2013; Wood et al., 2013b; Cano et al., 2014) has opened up new avenues in palaeomicrobiology.

4.1 Molecular clocks The ancient origin of parasitism is suggested by the deep-branching position of various parasitic lineages within the tree of life as well as the extrapolation of extant parasite host associations. In prokaryote and unicellular eukaryote, parasitic relationships might have already existed in the Precambrian, although so far no direct fossil evidence has been found. For metazoan parasites, for which the fossil constraints are better than they are for unicellular organisms, parasitism must have evolved at least for some groups during or slightly before the Cambrian explosion in the marine realm. This is corroborated by the earliest sign of parasitism by an unknown metazoan parasite in Cambrian brachiopods (Bassett et al., 2004) and body fossil remains of various pentastomid taxa from the CambrianeOrdovician (Castellani et al., 2011). Additional indications for parasitism are also found in other Lower Palaeozoic groups like Ordovician graptoloids (hemichordates) (Bates and Loydell, 2000) as well as in Silurian echinoderms (Franzen, 1974) and bivalves (De Baets et al., 2015a), although the exact identity of the culprits is unknown. Based on extrapolation of extant host-associations, the origin of parasitic flatworms and some lineages of parasitic nematodes have also been estimated to lie in the CambrianeOrdovician (Littlewood, 2006; Poinar, 2011a, 2015a). Since the assignment of Cambrian

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Kenneth De Baets and D. Timothy J. Littlewood

Cambroclavida (a group of enigmatic, phosphatized, hollow spine-shaped sclerites) to Acanthocephala (Qian and Yin, 1984) is unsubstantiated (Kouchinsky et al., 2012), the earliest confidently assigned ancient acanthocephalan remains are eggs derived from Quaternary archaeological sites (Fry and Hall, 1969; Noronha et al., 1994). The earliest metazoan helminth remains are circlets of hooks from Middle Devonian fishes (Upeniece, 2001), although their systematic affinity is still unclear (Littlewood and Donovan, 2003; De Baets et al., 2015a). So far no direct unequivocal evidence for metazoan parasites has been discovered in the Precambrian. Ediacaran fossils like Dickinsonia have occasionally been compared with Spinther (Wade, 1972; Conway Morris, 1981), an annelid parasite of sponges (Rouse, 2005b). This comparison proved to be superficial at best and they are now often interpreted to be more basal metazoans (Xingliang and Reitner, 2006; Sperling and Vinther, 2010), although the exact systematic position of Dickinsonia remains highly controversial (Retallack, 2007; Brasier and Antcliffe, 2008). More importantly, no evidence for a parasitic relationship of Dickinsonia with other taxa could be evidenced. A parasitic mode of life of Dickinsonia would be rather absurd too as it would mean the presence of hosts which would have to be considerably larger than Dickinsonia, which have remained unnoticed in the fossil record. Considering that bacteria, viruses and various other unicellular to multicellular eukaryotes have evolved before this time, many could have already evolved towards parasitism in the Precambrian. The discovery that the closest relative of parasitic apicomplexans is a coral symbiont might suggest that modern parasites may have started out as mutualistic metazoan symbionts before turning to parasitism (Moore et al., 2008). It has, therefore, been suggested that symbiotic/parasitic relationships in dinoflagellates and Apicomplexa might have extended back in evolutionary time to the earliest origins of Metazoa, which means that either as parasites or symbionts, these protists have been interacting with the metazoan immune system since their inception (Okamoto and McFadden, 2008). However, calibrating molecular clocks to test such hypotheses remains a challenge (Bensch et al., 2013). Parasitism-like life history patterns probably first evolved in the sea, but it is unclear if parasites closely tracked the terrestrialization of their hosts. In some cases this might have been true, as indicated by nematode remains in early diverging land plants from the Early Devonian (Poinar et al., 2008), although both plants and nematodes might have colonized the land considerably earlier based on molecular clock estimates (Clarke et al., 2011; Rota-Stabelli et al., 2013). In other cases it is less clear as the earliest

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fossil evidence for terrestrial parasitism in these lineages considerably predates the presumed origin of their host taxa (e.g. vertebrates or arthropods). However, various groups of terrestrial vertebrates (archosaurs, synapsids) were already parasitized in now extinct lineages leading up to currently infested host taxa (Poinar and Boucot, 2006; Da Silva et al., 2014). Although parasitism evolved in the sea, using this premise to constrain molecular clocks might be dangerous in particular cases; as is the case for various groups of nematodes parasitizing shallow marine to intertidal taxa, which have evolved convergently from terrestrial ancestors (Sudhaus, 2010). The fossil record can only provide minimum constraints on the origin of parasitism, but molecular clocks might be an alternative to dating important events without relying on recent evidence of parasiteehost associations or the evolutionary history of their hosts. The calibration of molecular clocks in pathogens with a poor fossil record like viruses, bacteria, protozoa (Bensch et al., 2013; Frías et al., 2013) or soft-bodied helminths (De Baets et al., 2015a) is not straightforward. The direct record is largely restricted to more recent Quaternary sites, particularly archaeological sites (Ara ujo et al., 2015; Mitchell, 2015) which can put important constraints on shallower nodes in phylogenies, although deeper nodes, particularly the root, in phylogenies are more crucial for dating (Warnock et al., 2012; Mello et al., 2014). Furthermore, most authors agree that multiple calibration points implemented faithfully across a phylogeny are ideal in achieving accurate and precise divergence estimates. However, these calibration points should be screened and selected a priori, rather than using posteriori selections methods, which evaluate congruence through cross-validation, as the latter can lead to selection of congruent, erroneous calibrations (Warnock et al., 2015). Nevertheless, the summary above shows that the body fossil record offers confident minimum constraints for various lineages of parasites, when critically evaluated. Various methods have been developed to estimate divergence times based on the stratigraphic distribution of fossil data (Wilkinson et al., 2011; Nowak et al., 2013; Heath et al., 2014), but most studies apply phylogenetic bracketing (M€ uller and Reisz, 2005; Benton and Donoghue, 2007) or probability functions that express some predefined perception of the degree to which fossil minima approximate the true time of divergence (Ho and Phillips, 2009). The latest tip-calibration or total evidence dating methods (Pyron, 2011; Ronquist et al., 2012; Wood et al., 2013a) allow fossils to be integrated into divergence time studies among their living relatives, using combined morphological and molecular datasets and evolutionary models. These have been shown, however, to yield

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unexpectedly old age estimates of clades (Arcila et al., 2015) and their performance needs to be more extensively tested. Furthermore, such methods might be difficult to apply to soft-bodied taxa as crucial morphological characters required to confidently place them in extant phylogenies might be absent or limited in fossil parasite specimens. Computed tomography will be important to reveal additional details of the morphology and structure of putative body fossils, which will make it possible to assign them more accurately to extant lineages. In some cases, the nearest free-living relatives have a good fossil record, which can be used to put constraints on early nodes in molecular clocks. Interestingly, this is not always the case. In some soft-bodied helminths, the body fossil record of parasitic forms is even richer (at least less poor) than that in their free-living relatives, such as amongst Platyhelminthes (Poinar, 2003; De Baets et al., 2015a) and Nematoda (Poinar, 2011a, 2015a). Their fossil record remains are rare in time and space due to their restriction to sites of exceptional preservation, but can potentially still be valuable to place constraints on the evolution of these groups as a whole. In the absence of reliable body fossils, characteristic traces or pathologies could potentially also be used to put constraints on certain nodes and computed tomography could also be possibly used to characterize those (Dittmar et al., 2011). Unfortunately, skeletal responses to parasitism are still comparatively poorly studied, particularly in extant taxa (Zibrowius, 1981; Ituarte et al., 2001, 2005; Keupp, 2012; Klompmaker et al., 2014). This makes interpretation of fossil traces even more open to interpretation as they could also have been made by a different group of organisms with a similar behaviour, but not necessarily closely related. It therefore probably makes more sense to avoid using them to constrain molecular clocks directly. Molecular clocks constrained by other types of evidence (e.g. body fossils or geological events) could however be used to test the appearances of these skeletal responses. Problematically, the fossil record does not yield body fossils or other remains for multiple lineages of unicellular pathogens or soft-bodied metazoan parasites (e.g. Myxozoa, Argulidae). In these cases, it is therefore necessary to look for and select suitable alternatives, or supplementary ways, to constrain the molecular clock (Bensch et al., 2013; De Baets et al., 2015a; Héritier et al., 2015). Such solutions potentially lie in the host fossil record or biogeographic events, which have left a footprint of divergence among evolutionary lineages. Unfortunately, host or biogeographic calibrations have not received the same scrutiny and refinement as fossil calibrations (Kodandaramaiah, 2011; De Baets and Donoghue, 2012; Parham et al.,

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2012; Hipsley and M€ uller, 2014). Biogeographic dating often relies on geochronologically or otherwise geologically dated events. As they are currently implemented, biogeographic calibrations and their age evidence are rarely if ever justified; they often assume the biogeography of living organisms is a faithful reflection of ancestral distribution, which is not always, or even rarely, the case as they might have been modified or even reset by subsequent events. Some exceptions have been suggested in parasites but these still need to be tested; for example, the cestode Nesolecithus and the nematode Nilonema have an apparent Gondwanaland origin with their present day distribution in Africa and South America (Gibson et al., 1987; Santos and Gibson, 2007). Furthermore, tectonic episodes are protracted and might have different impacts on lineages depending on their ecology. These limitations can be partially overcome or at least controlled like fossil calibrations, by implementing them in the most conservative way as probabilistic constraints that span an interval of time, which takes into account these factors (Warnock, 2014). Parasitologists often extrapolate extant parasiteehost or biogeographic relationships to estimate the evolutionary origin of parasites (Mejía-Madrid, 2013 for a review) or more rarely to calibrate molecular clocks, which can introduce a factor of circularity when testing hypotheses of evolutionary changes in parasiteehost associations or biogeographic distribution (Trewick and Gibb, 2010; Crisp et al., 2011; Kodandaramaiah, 2011; Hipsley and M€ uller, 2014). Although some of these hypotheses do stand the test of additional sampling of extant or fossil forms, others do not if quite different host associations or biogeographic distributions are recovered. Caution should be always taken as the fossil record also yields evidence of parasitic lineages and parasiteehost associations which are now clearly extinct (Upeniece, 2001; Poinar and Boucot, 2006; Castellani et al., 2011; Upeniece, 2011; Chen et al., 2014). Biogeographic distributions of their hosts and potentially that of their parasites might also have differed considerably in the past. Therefore, assumptions should be at least consistent with the fossil evidence and robust molecular clock estimates of their hosts. Not only does the fossil record provide direct and indirect evidence for the presence of certain parasite lineages, but it can also provide evidence for infection intensity, host response (developmental, pathological), novel (potentially extinct) host associations and parasite life cycles. Likewise, ancestral state reconstruction of host associations and life cycles (host use and complexity) from phylogenies, combined with calibrations can inform the interpretation of body fossils and inferred chronologies (Zhu et al., 2015). All factors considered, we should prefer to have an

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Kenneth De Baets and D. Timothy J. Littlewood

accurate timescale that might lack precision, than a precise timescale that lacks the necessary accuracy (De Baets et al., 2015a). Even if no suitable calibration points can be found, methods have been developed, which can compare the relative molecular rates of groups to test the hypotheses of co-divergences (Loader et al., 2007; Hibbett and Matheny, 2009; Loss-Oliveira et al., 2012; Silva et al., 2015).

4.2 HGT and ‘parasitic DNA’ Even for groups where no fossil biomolecules have been found, for example, viruses or symbionts, parasites can leave footprints in their hosts’ genomes (Gilbert and Feschotte, 2010; Thézé et al., 2011; Katzourakis, 2013; Koutsovoulos et al., 2014). Interrogation of genomes has made it possible to identify horizontal transfers of genetic elements (HGTs) in the deep history of living organisms. HGTs are the transfer of DNA between two nonvertically related individuals belonging to the same or different species (Sj€ ostrand et al., 2014). Some of these transfers retain an apparent parasitic role (Kidwell and Lisch, 2001) or become integrated into biochemical pathways that are functionally important in lineages that become parasitic (Alsmark et al., 2013). Comparison of such genomic signatures between species provides a means of determining their origins, diversification and change through time. Studies have focused particularly on ancient viruses (Gilbert and Feschotte, 2010; Thézé et al., 2011; Gifford, 2012; Herniou et al., 2013; Lee et al., 2013), typically revealing ‘hosteparasite’ interactions over prehistoric or geological timescales. There is increasing evidence that HGTs have left genomic signatures of other more highly organized symbionts like bacteria in their metazoan host genomes, too (Cerveau et al., 2011; Koutsovoulos et al., 2014). Things may be even more complicated as evidence of HGT may have occurred between various types of endosymbiotic bacteria (Duron, 2013) or viruses within their hosts (Niewiadomska and Gifford, 2013). There is no physical ‘fossil record’ of these viruses or signatures (Katzourakis and Gifford, 2010; Katzourakis, 2013), and their long unchanged history is inferred such that they cannot be referred to as genomic ‘fossils’ as such. However, further evidence of historical hoste parasite interactions will undoubtedly arise from future genomic studies of both hosts and parasites, although an understanding of the role of HGT in eukaryotes is still in its infancy (Hirt et al., 2015). HGT events are common in prokaryotes and many microbial eukaryotes, but are expected to become more commonly detected in multicellular

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eukaryotes as more is known about their genomes (Andersson, 2005). With microbial phylogenies, HGTs are important in revealing which evolutionary lineages were concurrent and when speciation (or broader divergence) events took place. By explicitly modelling the evolution of genes present in genomes, Sz€ ollTsi et al. (2012) provided a chronologically ordered phylogeny for cyanobacteria, validated against the groups’ good microfossil record, thus showing that their methods can reveal and use HGTs as a source of information on timing (or at least chronology) of evolutionary events. Focusing on microbial eukaryotes, Alsmark et al. (2013) showed the pattern of HGTs retained after parasite diversification are likely to be functionally important for the parasites (e.g. in kinetoplastids and apicomplexans). Similarly, there is strong evidence that multiple HGT events have promoted the plant parasitism ability in some nematodes (Danchin et al., 2010). There is increasing evidence that the role of HGTs in eukaryote evolution is important, particularly in the evolution of resistance, and it does not seem overly speculative to predict that signatures from hosteparasite interactions will be found in more genomes. Further interrogation will reveal lineages of parasites with genomic signatures of their long-associated histories with their host groups, and vice versa; for example, Richards et al. (2011); Wijayawardena et al. (2013); Davis and Xi (2015). In turn, this evidence will provide indications as to when particular lineages came into contact with one another, but the success of these leads in revealing accurate records of historical interactions depends on greater study. Some recent claims of HGT in multicellular parasites (e.g. schistosomes) have been discredited, revealing the need to be wary of technical artifacts and gene conservation issues before claims of HGT can be verified (Wijayawardena et al., 2015).

5. FUTURE PERSPECTIVES Various new advances in ancient biomolecule detection and characterization (Briggs and Summons, 2014) including aDNA (Dittmar, 2009, 2014; Wood et al., 2013b; Dittmar, 2014; Shapiro and Hofreiter, 2014; Hofreiter et al., 2015), palaeoproteomics (Hofreiter et al., 2012), novel development in molecular clock methodologies (Parham et al., 2012; Ho, 2014; W€ orheide et al., 2015) and new possibilities for the critical evaluation and nondestructive analysis of 3D fossil structures by computed tomography (Cunningham et al., 2014a,b; Sutton et al., 2014) offer many new prospects and perspectives in palaeoparasitology.

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ACKNOWLEDGEMENTS We are very grateful to Andrea Waeschenbach and Rod Bray for constructive comments on an earlier draft of the manuscript. The initial research leading to this article was partially funded by an SNF-grant for Prospective Researchers to KDB (141438).

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