Testing cospeciation through large-scale cophylogenetic studies

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ScienceDirect Testing cospeciation through large-scale cophylogenetic studies Astrid Cruaud and Jean-Yves Rasplus Insects are involved in a multitude of interactions with other organisms, which make them ideal models for large-scale cophylogenetic studies. Once phylogenies of interacting lineages have been inferred, there are a number of questions we may wish to ask, such as what was the relationship between the partners in the past? Have they co-evolved for thousands or millions of years, or has one of the partners switched among different host species? To answer such questions, researchers may conduct cophylogenetic analysis, to explore the relationships between the phylogenies of interacting lineages and determine whether the match is significant or find explanations for observed differences. When combined with dating analyses, cophylogenetic analyses may support cospeciation of the partners or phylogenetic tracking. As they may reveal dynamics of host-pathogen coevolution, cophylogenetic studies may also help tackle global health issues (e.g. document the spread of disease causing pathogens). Cophylogenetic studies of parasitoids and their insect hosts may also help identify effective biocontrol agents. With the advent of next generation sequencing technologies and keeping in mind that systematic errors may occur, cophylogenetics will benefit from better-resolved trees, allowing more accurate reconciliation. However as trees become larger, current algorithms also become more computationally challenging. Nevertheless, both theoretical and methodological developments are leading to more accurate and powerful tests of cospeciation through cophylogenetic analysis. Address INRA, UMR1062 CBGP, F-34988 Montferrier-sur-Lez, France Corresponding author: Cruaud, Astrid ([email protected])

Current Opinion in Insect Science 2016, 18:53–59 This review comes from a themed issue on Insect phylogenetics Edited by Gregory W Courtney and Brian M Wiegmann For a complete overview see the Issue and the Editorial Available online 19th October 2016

with other organisms such as bacteria, microsporidia, fungi, plants, nematodes, and vertebrates, which make them great models for large-scale cophylogenetic studies (Box 1) and, more generally, coevolution. Patterns of cospeciation have been observed in multiple systems that include insect lineages. Generally, cospeciation is more frequently expected when the life histories of the two interacting lineages are tightly linked such as for vertically transmitted symbionts and their insect hosts, or when interactions are species specific. Mutualistic interactions between insects and their endosymbiotic bacteria are ubiquitous and occur in many insect groups (e.g. [1]). These interactions facilitate the use by the insects of nutritional resources from various difficult to digest sources, such as sap, wood, etc. For Hemipteran insects, endosymbionts provide nutrients to their insect hosts that feed on sap, a resource that miss essential amino acids. In these obligate interactions, congruence among phylogenies has been demonstrated (aphids and Buchnera [2], leafhoppers and Sulcia/Baumannia [3], stinkbugs (Plataspidae) and a specific gut bacterium (g-Proteobacteria) that is vertically transmitted from the mother to her developing eggs [4]. Strict cospeciation also occurs between cockroaches or termites and their obligate endosymbionts (Blattabacterium) and/or gut microbiomes that exhibit a cellulolytic and diazotrophic activity [5,6]. Another case of mutualistic interaction in which cospeciation may be expected is mimicry (e.g. between species of Heliconius butterflies H. erato and H. melpomene). For this example, results remain unclear. The first phylogenetic analyses found contrasting histories with topological and temporal incongruence that argued against codivergence [7]. However, using coalescent based methods and cutting-edge cophylogenetic methods, Cuthill and Charleston [8] concluded that the evolutionary history of H. erato and H. melpomene was compatible with a number of temporally congruent codivergence events.

http://dx.doi.org/10.1016/j.cois.2016.10.004 2214-5745/# 2016 Elsevier Inc. All rights reserved.

Insect groups involved in patterns of cospeciation Insects are one of the most successful groups of animals on Earth. They are involved in a multitude of interactions www.sciencedirect.com

Plant-herbivore or host-parasite coevolution can also result in patterns of cospeciation, though much less frequently. Mutualistic interactions involving insects are diverse and ecologically important [9]. In these highly specialized relationships, the two interacting species mutually benefit from their interactions. A few plant genera (Ficus, Yucca, and Glochidion) are exclusively pollinated by obligate seed-parasitic insects (Agaonidae wasps, Prodoxidae and Epicephala moths respectively). Insects pollinate the flowers and oviposit in the plant ovaries where larvae Current Opinion in Insect Science 2016, 18:53–59

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Box 1 Glossary When starting to compare the evolutionary history of interacting lineages, one may stumble on the following terms especially since they are frequently used interchangeably: codivergence, coevolution, cophylogeny, cospeciation. This box attempts to give what we believe are consensual definitions of these terms and others, that may appear confusing. Coadaptation: Microevolution of two or more interacting species in response to reciprocal selection between them [49]. Codivergence: The parallel divergence of interacting lineages. Codiversification: Correlative diversification of two or more interactive lineages or organisms. Speciation events in one lineage are correlated with speciation events in a second lineage [30]. Coevolution: Reciprocal natural selection occurring during reciprocal evolutionary interaction between two or more organisms. Cophylogenetics: field of research that focuses on the macro scale coevolutionary associations formed between the phylogenies of interacting lineages [50]. Cophylogeny = cophylogenetic analysis explores the relationships between the phylogenetic trees of interacting lineages. In most analyses, the goals are to determine whether the match/congruence between the two (or more) trees is significant and to find the best explanation for the differences between the trees [20]. Cospeciation: The matching of speciation events and their cooccurrence upon the time between two or more interacting lineages. Phylogenetic tracking: A pattern in which cladogenesis occurs in parallel in two interacting lineages of organisms, but the speciation events are not synchronous (i.e. one lineage speciates first and is followed by speciation in the other).

subsequently feed on a subset of the developing seeds. In these nursery pollination mutualisms, only a few studies have investigated the level of cocladogenesis between sparsely sampled phylogenies of the mutualistic partners. Cophylogenetic analyses of yuccas and their pollinator moths showed congruence between the phylogenies, though this pattern may be better explained by biogeographic factors than by coevolution (as within a lineage, yucca species and their hosts mostly occur in allopatry) [10]. Both cospeciation and host shifts have played an important role throughout the evolutionary history of the Glochidion and Epicephala moth system [11]. Finally, the largest cophylogenetic study published so far that focussed on the fig–fig wasps mutualism [12] highlighted long-term cospeciation between the partners (Box 2). Regarding parasites, studies have been published on ectoparasites of animals such as chewing or sucking lice that develop on the body of birds (ducks, doves, flamingos, pelecans, penguins, pigeons, seabirds or toucans) or mammals (primates, rodents). Cospeciation patterns have been demonstrated between sucking lice and heteromyid rodents [13], chewing lice and marine birds [14] and body louse and New World doves [15]. However, for most groups of lice and their vertebrate hosts, Current Opinion in Insect Science 2016, 18:53–59

phylogenetic congruence is not the rule. Cophylogeny between parasitoids and their insect hosts has been rarely investigated (e.g. [16]), though such studies may help to set up effective biocontrol programs (e.g. reduce unintended effects). On a more general note, most cophylogenetic studies are conducted on two-lineage systems and only a few focused on more complex systems (e.g. moth/parasitoids/plants [17]), though this may help to better understand dynamics among multiple trophic layers in an ecosystem or specialized interaction.

Analytical approaches used in cophylogenetic studies Current methods are divided into two main groups: ‘event based’ and ‘global fit’ methods (see e.g. de Vienne et al. [18] and Filipiak et al. [19]). Event based methods consist of mapping the ‘dependent’ (parasite/symbiont, etc.) phylogeny onto the ‘independent’ (host) phylogeny, to analyse the congruence between the pair of trees, and reconcile their shared evolutionary history. Reconciliation generally considers four evolutionary events: codivergence, duplication, host switch and loss, and supposes that parasite/symbiont, etc. may only inhabit a single host. In parsimonious event-based methods, each event is assigned a penalty score and algorithms are developed to infer a minimum cost mapping, which aims to represent the most likely shared history between the pair of phylogenetic trees [20,21,22]. When timing information is available, software can differentiate compatible and incompatible host switches and propose alternative minimum cost scenarios for reconciliation (e.g. [23]). Obviously, event cost value, which is difficult to evaluate a priori, may impact the solution. Therefore, new methods have been developed to explore the space of cost vectors. Coevolution Assessment by a Likelihood-free Approach (COALA) tries to estimate the frequency of different evolutionary events based on an Approximate Bayesian Computation approach [24]. Starting from the phylogenies of the interacting lineages and a prior probability distribution of each event, COALA generates a number of simulated ‘dependent’ trees using different probabilities for each event. Trees are then compared with the known ‘dependent’ tree and parameter values leading to trees closest to the known tree are kept, while others are rejected. Optimal reconciliations between the two input trees are then proposed. Recent work has focused on the development of new algorithms that are not too computationally expensive to reconcile trees that become larger and larger with the advent of NGS technologies (e.g. [21,24,25]). Algorithms have also been developed to handle the confounding effects of widespread parasites (parasites that are associated with different and sometimes phylogenetically distant hosts) [26] and to address the need for quantitative measures of phylogenetic uncertainty [24]. A major criticism of event-based methods is that comparison of www.sciencedirect.com

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Box 2 Cospeciation in figs and fig wasps Co-speciation may exist in a few obligate mutualistic partnerships. Among groups that exhibit intimate interactions, figs and their pollinating fig wasps may represent the first demonstrated case of long-term (75 myr) codivergence in an insect–plant association. The fig–fig wasp mutualism is an important focal association for the study of co-speciation and co-diversification [51,52]. To accurately determine the extent of shared evolutionary history between figs and fig pollinating wasps, phylogenies of both partners must be reconstructed reliably. However, until now, testing cospeciation of figs and fig wasps has been hampered by the poor resolution of the deep nodes of both phylogenies. In all phylogenetic studies of the partners, the relationships among the fig sections and the agaonid genera (i.e. the backbone topology) were difficult to resolve [53,54]. Using ca 200 pairs of interacting fig and fig wasp species and about 5.5 kb DNA sequence for each species, Cruaud et al. [12] tested cospeciation between figs and fig wasps. However, the analysis was hampered by the poor resolution of the phylogenies of the mutualists and possibly also long-branch attraction artifacts for the fig trees. The phylogeny of figs was globally congruent with previous hypotheses, but relationships of deeper nodes were poorly supported. Similarly, the phylogeny of the fig pollinators (belonging to the chalcid family Agaonidae) was not resolved and the relationships among the major clades were unclear. Further studies are thus needed to end up with a clear scenario of what happened during the evolutionary history of this unique association.

Conosycea

Americana

Waterstoniella Eupristina Deilagaon

Pegoscapus Current Opinion in Insect Science

Expanded views of different parts of the host (Ficus) and pollinator (Agaonidae) trees published by Cruaud et al. [12] showing different degrees of congruence/divergence. Top: Congruence between Ficus from the section Conosycea (Asia) and their three genera of pollinators (Eupristina, Deilagaon, Waterstoniella) is higher than between (Bottom) Ficus from the section Americana (Neotropics) and the genus Pegoscapus, though all these fig trees belong to the subgenus Urostigma (big stranglers). Patterns must be nevertheless considered with caution, as some nodes are poorly resolved (Black squares: BP > 70% and PPMrBayes or PPBEAST > 0.95; white squares: BP > 70% or PPMrBayes or PPBEAST > 0.95).

patterns alone does not include all of the evidence required to test for cospeciation [18]. Ideally, different types of method and evidence should be used to assess possible cospeciation among interacting lineages. In all cases, results should be interpreted with caution, keeping in mind that congruence between trees (regardless of how it is evaluated) does not necessarily imply cospeciation. Global-fit methods do not propose evolutionary scenarios but quantify the degree of congruence between two trees. Some also identify associations that contribute to congruence [27]. Until recently, these methods were favoured as they could accommodate larger trees than event based methods and were able to manage one-to-multiple www.sciencedirect.com

associations [28]. Many global-fit methods are currently available. These methods can test for similarity or independence of tree topologies and use either tree topology, distance matrices or alignment to perform tests [18]. Powerful approaches have been implemented, for example PACo, for ‘‘Procrustean Approach to Cophylogeny’’. PACo provides a superimposition plot enabling a graphical assessment of the fit of the ‘dependent’ phylogeny onto the ‘independent’ phylogeny. A goodness-of-fit statistic is also returned.

What does a pattern of congruence between phylogenies tell us? The aim of cophylogenetic analyses is to determine whether the phylogenies of both sets of participants mirror Current Opinion in Insect Science 2016, 18:53–59

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Figure 1

Sampling of hosts and associates • As much as possible, try to be exhaustive (sample extant + extinct lineages) • Do not forget outgroups (not too distantly related) • When possible rely on expert taxonomists for accurate identification Or use accurate databases for DNA based identification

Choice of DNA markers and sequencing • • • •

Extract DNA just after field work Use non destructive DNA extraction (if possible and required; e.g., species complexes) Avoid mtDNA, chloroplastic DNA and rRNA Sequence multiple markers (e.g., amplicon, exome capture, RAD-seq )

Phylogenetic inference • •

Remove paralogs and non-homologous sequences/contaminants Gene tree/species tree VS supermatrix approaches

many markers does not necessarily mean more accurate phylogeny (systematic bias) use appropriate models consider among-site variation in the rate of substitution (Γ distribution, CAT model) partitioning schemes and nt substitution models may be estimated from the data test for possible heterogeneous lineage evolutionary rates

• • •

Use accurate methods of species delimitation if required Ask taxonomists for a feedback on your results (integrative approach) Compare results obtained with different methods

Dating analyses • • • •

Together with phylogenetic inference or a posteriori Use accurate calibration and priors New methods allow dating analyses without fossils Compare results obtained with different methods

Cophylogenetic analyses • •

Compare event-based and global-fit methods Remember that congruence does not imply cospeciation

temporal congruence must be tested

• •

Remember that cospeciation should not be construed as coevolution Use other lines of evidence to interpret results of cophylogenetic analyses

evaluate plausibility of tree reconciliation using ecological, biogeographical etc. data Current Opinion in Insect Science

Suggested workflow to test cospeciation through large-scale cophylogenetic studies.

each others, an hypothesis known as the ‘Fahrenholz’s rule’ [29]. Pattern of strict congruence may reflect reciprocal genetic changes between interacting organisms. Cospeciation requires that first, tree topologies are congruent, and second, timing of speciation in both lineages, inferred from these trees, is synchronous (a correlation may only imply phylogenetic tracking). Consequently, rigorous tests of cospeciation require: first, exhaustive Current Opinion in Insect Science 2016, 18:53–59

sampling of hosts and associates (extant and when possible extinct), second, reliable and fully resolved phylogenetic hypotheses, and finally accurate cophylogenetic and dating analyses (Figure 1). It is important to point out that cospeciation should not be construed as coevolution because reciprocal selection or adaptation may not be involved. Demonstration of a strict www.sciencedirect.com

Large-scale cophylogenetics Cruaud and Rasplus 57

pattern of congruence between phylogenies is not enough to certify that cospeciation did/does occur. Such a pattern can be produced without any coevolutionary processes being involved [30,31]. A pattern of strict congruence may occur when speciation in the interacting lineages is due to barriers to dispersal formed by geologic events (vicariance). Host shifts [32] as well as vertical transmission may also lead to patterns of congruence without any evidence of coevolution. Finally, matching phylogenetic patterns can simply result from sequential evolution, in which the evolution of one lineage influences the evolution of the other but not vice versa [33]. Time calibrated phylogenies of lineages provide a temporal context for the duration of their interactions over macroevolutionary time. However, evidence for the persistence of associations do not provide evidence for coadaptation, and complementary studies are necessary to put ‘coadaptive flesh on the cophylogenetic bones’ [34].

What next? Next generation cophylogenetic studies Accurate topologies are of prime importance to test cospeciation and it is now acknowledged that data sets based on single or a few molecular markers cannot reliably infer phylogenies of ancient interacting organisms. Furthermore, mtDNA or organelle genes can produce confounding topologies due to introgression or selection [35] and paralogy of rDNA genes may also impede phylogenetic reconstruction [36]. Consequently, numerous nuclear markers are often necessary to accurately infer species-level phylogenies and better assess congruence between topologies. Advances in NGS technologies allow the easy acquisition of large nucleotide data sets that can be used for phylogenetic purposes [37]. It is noteworthy that while sequencing more markers should not be an issue, collecting samples for large-scale studies may be more and more difficult. Indeed, to reduce the risk of biopiracy, many countries have imposed restrictive access regulations even to academic researchers. Nevertheless, a positive attitude toward international collaborations for non-commercial research was shown through the development of the Nagoya protocol [38]. Advances in methodologies for phylogenetic inference should also result in more accurate trees, though large data sets can be subject to hidden, or difficult to detect, systematic bias [39,40]. When data sets are very large, parameter estimates have very little uncertainty. If the model used is inconsistent for a specific bias, large data sets are likely to make the problem worse [41]. Systematic errors are due to incorrect model assumptions (oversimplified models do not accurately describe the processes that generated the data). Some biases, such as longbranch attraction due to accelerated evolutionary rates in unrelated lineages, are sometimes hard to detect and www.sciencedirect.com

correct, but here again progress has been made to help circumvent such issues [42]. This is important to consider because interacting partners may have very different generation times or population sizes that may lead to differential co-adaptation and also different rates of molecular evolution. Lineages of parasites may thus display highly heterogeneous lineage-specific evolutionary rates leading to possible reconstruction bias and incorrect tree reconciliation. Regarding dating analyses, advances in Bayesian divergence time methods, and increased computational power improve the reliability of timetrees based on thoroughly sampled large data sets [43,44,45]. Recent analytical developments that enable estimates of divergence times via biogeographic processes [46] may also contribute to better inferences of the tempo of some insect–macro-organisms interactions. Indeed, many insect groups leave few or no known fossils. As is true for all macroevolutionary investigations, including cophylogenetic methods, models of sequence evolution or clock models, will always be approximation of the complex reality of historical processes and interactions, and so the results of large-scale cophylogenetic studies should be interpreted with caution. A detailed knowledge of any ‘model system’ under study is critical and, in this genomic era, expert taxonomists remain crucial to the accuracy of any such investigation. Indeed as suggested by Page et al. [47], an adequate alpha-taxonomy for both partners is a prerequisite for accurate cophylogenetic studies. Taxonomists are a primary source of information on species, their relationships, and species concepts. Indeed, difference in species concepts that may exist between the interacting organisms (e.g. Bacteria versus macro-organisms, but also among macro-organisms such as between plants and insects) is rarely addressed. Calibrating species levels in both partners is difficult, and would require detailed study of species limits for both. For example, the interaction may be intraspecific for the host and specific for the parasite. Consequently, inclusion of multiple populations from the ‘host’ lineage as well as individuals of the ‘parasite’ associated to each of these populations may be necessary to find evidence for cospeciation in such a system. With progress in coalescent-based species delimitation methods, such issues should be addressable using large data sets in the near future [48].

Acknowledgements We thank Gregory W. Courtney and Brian Wiegmann for their careful review of the manuscript and helpful comments.

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