- Email: [email protected]
Born to be Wild – Don’t Forget the Invertebrates
TREPAR 1426 No. of Pages 2
Letter
Born to be Wild – Don’t Forget the Invertebrates Michael J. Wilson,1,* Elena S. Ivanova,2 and Sergei E. Spiridonov2
changes associated with adopting a parasitic lifestyle. Parasitologists often compare genomes of their preferred parasite with the model nematode, Caenorhabditis elegans, even though the two organisms may be dissimilar. An excellent comparative model would be the facultative slug parasitic nematode Phasmarhabditis hermaphrodita and C. elegans. The nematodes are closely related phylogenetically, feed on decaying plant material, and dauer larvae of both associate with slugs. However, whereas C. elegans merely uses slugs for transport (phoresy), dauer larvae of P. hermaphrodita have the ability to develop and feed on slug tissue [5]. The nematodes are a particularly rich source of invertebrate parasites that infect many taxa. The evolutionary relationships and the suggestion that certain vertebrate parasites may have evolved via invertebrate parasitism makes them particularly worthy of study [6] (Figure 1).
Parasitology research mostly aims to control parasites of humans and domesticated animals. Recently, many scientists have realized much can be learned by studying wildlife parasites. To this end, Trends in Parasitology published two special issues comprising some of the most interesting, topical science relating to wildlife parasitology [1]. The emphasis of the published articles was almost exclusively on parasites that use vertebrate animal hosts. Here, we argue that progress in parasitology could be accelerated if more parasitologists studied parasites that use invertebrates as definitive hosts. Dynamics of Coinfection Another topic considered by wildlife paraHigh Diversity Means Better sitologists is coinfection and, to this end, Model Systems The diversity of invertebrate animals is vast Rynkiewicz et al., consider the applicability compared with vertebrates. According to a ecosystem ecology tools for parasitology recent study, the phylum Craniata (verte- [7]. Because the diversity of macroparabrates) comprises 64 832 species, a mere sites of vertebrate animals is limited, these 4% of total animal biodiversity [2]. This authors considered all pathogenic microprobably represents a substantial overesti- organisms as parasites, necessitating mate as it is likely there are many more study of the whole host–microbiome, undescribed invertebrate than vertebrate which the authors admitted could result species. In spite of this, most animal biol- in ‘potentially overwhelming levels of comogists work with vertebrate animals and plexity’. It should be noted that most this phenomenon has been referred to as ecosystem ecology has been developed ‘Institutionalised Vertebratism’ [3]. Most using macroflora and fauna. An ideal invertebrate animals have parasites and model for studying ecosystem tools for their great diversity enables identification coinfection could be the spirobolid and of individual host–parasite systems ideal spirostreptid millipedes. These invertefor studying specific areas of fundamental brates have a relatively simple anatomy, parasitology. However, while the lack of but support a surprising diversity of mactaxonomic expertise for parasites of verte- roparasites [8], and we have observed up brates has been noted [4], the situation is to ten parasite species cohabiting in a single host millipede. even worse for the invertebrates.
parasitology, issues addressed include the threats posed to native wildlife by invaders acting as reservoirs of parasites or introducing new species of parasites [9]. Among the most important invertebrate invaders are those that damage agricultural crops in their new range, and there is evidence that release from parasites promotes success in their new territories [10]. This raises the intriguing possibility of introducing the parasites into the new territory to control the invasive pests. A successful example is use of the nematode parasite Beddingia siricidicola to manage the wood wasp Sirex noctilio. This European wasp was introduced into Australia in the 1950s and became a serious pest of pine plantations. The nematode was introduced as a control agent in the 1970s and since has largely controlled the invasive wasp [11].
Practical Advantages
The short life cycles of invertebrate animals (sometimes days) allow the effects of parasites to be studied over many generations within a typical research grant period. Also, the small size and low motility of many non-flying invertebrates means ecology can be studied in laboratory microcosms, or small field plots. This enables specific hypotheses to be tested using replicated plots. An example where such population ecology was used for a practical purpose was the development of population models to control sciarid fly pests in glasshouses using the insect parasitic nematode, Steinernema feltiae [12]. However, we believe similar approaches could be used for tackling many fundamental questions in host parasite ecology. For example, effects of host density on parasite transmission could be studied by experimentally manipulating host insect populations in plots by, for example, applying varying levels of insecticides. This last point is facilitated by another key advantage; in nearly all cases, experimental use of invertebrate animals is not Managing Invasive Species The Evolution of Parasitism covered by animal welfare legislation. A theme frequently addressed by para- Biological invasions represent a major While universally accepted as necessary, sitologists is determining the genetic threat to biodiversity. In terms of such legislation can increase the financial
Trends in Parasitology, Month Year, Vol. xx, No. yy
1
TREPAR 1426 No. of Pages 2
and administrative costs of parasitology research considerably.
Inv_a
1
Inv_d
s Phasmarhabdi e Heterorhabdida ea gyloid n o r t S Angio stomada e Agfidae
Sphae rularioidea Aphe lenchoide a Dril one m atoidea Str Alanin emadae ong yloi did a e (Rhabdiasidae?) Stein erne ma dae Allo io nem a d a e
Vert Inv_di
Inv_mp Inv_ip Vert Inv_m Inv_m
*Correspondence: [email protected] (M.J. Wilson). http://dx.doi.org/10.1016/j.pt.2015.09.002 References 1. Camejo, A. and Loughlin, D.T. (2015) Born to be wild. Trends Parasitol. 31, 121–122 2. Zhang, Z.Q. (2011) Animal biodiversity: an introduction to higher-level classification and taxonomic richness. Zootaxa 3148, 7–12
Rhabdina
ea oid a mat e ide n om ato m e Rans on Rhig idea Oxyuro a atoide Thelastom
3. Leather, S.R. (2009) Institutional vertebratism threatens UK food security. Trends Ecol. Evol. 24, 413–414 4. Hoberg, E.P. et al. (2015) An integrated parasitology: revealing the elephant through tradition and invention. Trends Parasitol. 31, 128–133 5. Wilson, M.J. et al. (1993) The rhabditid nematode Phasmarhabditis hermaphrodita as a potential biological control agent for slugs. Biocontrol Sci. Technol. 3, 503–511 6. Blaxter, M. and Koutsovoulos, G. (2015) The evolution of parasitism in Nematoda. Parasitology 142, S26–S39
Inv_i Inv_i Inv_a Inv_m Vert
7. Rynkiewicz, E.C. et al. (2015) An ecosystem approach to understanding and managing within-host parasite community dynamics. Trends Parasitol. 31, 212–221
Tylenchina
Rhabdida
Plecda
Orders
Inv_d
Spirurina
Suborders ae rcid oce r g a Cre
AgResearch, Ruakura Research Centre, Hamilton 3240, New Zealand 2 Centre for Parasitology of the A.N. Severtsov Institute of Ecology and Evolution, RAS 119071, Moscow, Russia
Inv_ip Inv_m
8. Spiridonov, S.E. (1989) New species of Rhigonematida (Nematoda) from the Cuban spirobolid Rhinocricus sp. (Diplopoda). Folia Parasitol. 36, 71–82 9. Dunn, A.M. and Hatcher, M.J. (2015) Parasites and biological invasions: parallels, interactions, and control. Trends Parasitol. 31, 189–199 10. Ross, J.L. et al. (2010) The role of parasite release in invasion of the USA by European slugs. Biol. Invas. 12, 603–610 11. Bedding, R.A. and Iede, E.T. (2005) Application of Beddingia siricidicola for Sirex woodwasp control. In Nematodes as Biocontrol Agents (Grewal, P.S. et al., eds), pp. 385–399, CABI Publishing 12. Fenton, A. et al. (2002) Optimal application strategies for entomopathogenic nematodes: integrating theoretical and empirical approaches. J. Appl. Ecol. 39, 481–492
Figure 1. Phylogenetic Relationships of Nematode Parasites of Invertebrates in the Orders Rhabditida and Plectida Showing Multiple Independent Acquisitions of Parasitism in Diplopods, Annelids, and Terrestrial Mollusks. Phylogenetic links of nematodes that parasitize vertebrates are also highlighted (*, probable common ancestor of such groups). Abbreviations: Inv_a, parasitism in annelid host; Inv_di, parasitism in insect and diplopod host; Inv_d, parasitism in diplopod host; Inv_i, parasitism in insects; Inv_ip, nematode pathogenic for insects (vectors of pathogenic bacteria); Inv_m, parasitism in mollusk host; In_mp, nematode pathogenic for mollusks; Vert, parasitism in vertebrates.
2
Trends in Parasitology, Month Year, Vol. xx, No. yy
Letter
Born to be Wild – Don’t Forget the Invertebrates Michael J. Wilson,1,* Elena S. Ivanova,2 and Sergei E. Spiridonov2
changes associated with adopting a parasitic lifestyle. Parasitologists often compare genomes of their preferred parasite with the model nematode, Caenorhabditis elegans, even though the two organisms may be dissimilar. An excellent comparative model would be the facultative slug parasitic nematode Phasmarhabditis hermaphrodita and C. elegans. The nematodes are closely related phylogenetically, feed on decaying plant material, and dauer larvae of both associate with slugs. However, whereas C. elegans merely uses slugs for transport (phoresy), dauer larvae of P. hermaphrodita have the ability to develop and feed on slug tissue [5]. The nematodes are a particularly rich source of invertebrate parasites that infect many taxa. The evolutionary relationships and the suggestion that certain vertebrate parasites may have evolved via invertebrate parasitism makes them particularly worthy of study [6] (Figure 1).
Parasitology research mostly aims to control parasites of humans and domesticated animals. Recently, many scientists have realized much can be learned by studying wildlife parasites. To this end, Trends in Parasitology published two special issues comprising some of the most interesting, topical science relating to wildlife parasitology [1]. The emphasis of the published articles was almost exclusively on parasites that use vertebrate animal hosts. Here, we argue that progress in parasitology could be accelerated if more parasitologists studied parasites that use invertebrates as definitive hosts. Dynamics of Coinfection Another topic considered by wildlife paraHigh Diversity Means Better sitologists is coinfection and, to this end, Model Systems The diversity of invertebrate animals is vast Rynkiewicz et al., consider the applicability compared with vertebrates. According to a ecosystem ecology tools for parasitology recent study, the phylum Craniata (verte- [7]. Because the diversity of macroparabrates) comprises 64 832 species, a mere sites of vertebrate animals is limited, these 4% of total animal biodiversity [2]. This authors considered all pathogenic microprobably represents a substantial overesti- organisms as parasites, necessitating mate as it is likely there are many more study of the whole host–microbiome, undescribed invertebrate than vertebrate which the authors admitted could result species. In spite of this, most animal biol- in ‘potentially overwhelming levels of comogists work with vertebrate animals and plexity’. It should be noted that most this phenomenon has been referred to as ecosystem ecology has been developed ‘Institutionalised Vertebratism’ [3]. Most using macroflora and fauna. An ideal invertebrate animals have parasites and model for studying ecosystem tools for their great diversity enables identification coinfection could be the spirobolid and of individual host–parasite systems ideal spirostreptid millipedes. These invertefor studying specific areas of fundamental brates have a relatively simple anatomy, parasitology. However, while the lack of but support a surprising diversity of mactaxonomic expertise for parasites of verte- roparasites [8], and we have observed up brates has been noted [4], the situation is to ten parasite species cohabiting in a single host millipede. even worse for the invertebrates.
parasitology, issues addressed include the threats posed to native wildlife by invaders acting as reservoirs of parasites or introducing new species of parasites [9]. Among the most important invertebrate invaders are those that damage agricultural crops in their new range, and there is evidence that release from parasites promotes success in their new territories [10]. This raises the intriguing possibility of introducing the parasites into the new territory to control the invasive pests. A successful example is use of the nematode parasite Beddingia siricidicola to manage the wood wasp Sirex noctilio. This European wasp was introduced into Australia in the 1950s and became a serious pest of pine plantations. The nematode was introduced as a control agent in the 1970s and since has largely controlled the invasive wasp [11].
Practical Advantages
The short life cycles of invertebrate animals (sometimes days) allow the effects of parasites to be studied over many generations within a typical research grant period. Also, the small size and low motility of many non-flying invertebrates means ecology can be studied in laboratory microcosms, or small field plots. This enables specific hypotheses to be tested using replicated plots. An example where such population ecology was used for a practical purpose was the development of population models to control sciarid fly pests in glasshouses using the insect parasitic nematode, Steinernema feltiae [12]. However, we believe similar approaches could be used for tackling many fundamental questions in host parasite ecology. For example, effects of host density on parasite transmission could be studied by experimentally manipulating host insect populations in plots by, for example, applying varying levels of insecticides. This last point is facilitated by another key advantage; in nearly all cases, experimental use of invertebrate animals is not Managing Invasive Species The Evolution of Parasitism covered by animal welfare legislation. A theme frequently addressed by para- Biological invasions represent a major While universally accepted as necessary, sitologists is determining the genetic threat to biodiversity. In terms of such legislation can increase the financial
Trends in Parasitology, Month Year, Vol. xx, No. yy
1
TREPAR 1426 No. of Pages 2
and administrative costs of parasitology research considerably.
Inv_a
1
Inv_d
s Phasmarhabdi e Heterorhabdida ea gyloid n o r t S Angio stomada e Agfidae
Sphae rularioidea Aphe lenchoide a Dril one m atoidea Str Alanin emadae ong yloi did a e (Rhabdiasidae?) Stein erne ma dae Allo io nem a d a e
Vert Inv_di
Inv_mp Inv_ip Vert Inv_m Inv_m
*Correspondence: [email protected] (M.J. Wilson). http://dx.doi.org/10.1016/j.pt.2015.09.002 References 1. Camejo, A. and Loughlin, D.T. (2015) Born to be wild. Trends Parasitol. 31, 121–122 2. Zhang, Z.Q. (2011) Animal biodiversity: an introduction to higher-level classification and taxonomic richness. Zootaxa 3148, 7–12
Rhabdina
ea oid a mat e ide n om ato m e Rans on Rhig idea Oxyuro a atoide Thelastom
3. Leather, S.R. (2009) Institutional vertebratism threatens UK food security. Trends Ecol. Evol. 24, 413–414 4. Hoberg, E.P. et al. (2015) An integrated parasitology: revealing the elephant through tradition and invention. Trends Parasitol. 31, 128–133 5. Wilson, M.J. et al. (1993) The rhabditid nematode Phasmarhabditis hermaphrodita as a potential biological control agent for slugs. Biocontrol Sci. Technol. 3, 503–511 6. Blaxter, M. and Koutsovoulos, G. (2015) The evolution of parasitism in Nematoda. Parasitology 142, S26–S39
Inv_i Inv_i Inv_a Inv_m Vert
7. Rynkiewicz, E.C. et al. (2015) An ecosystem approach to understanding and managing within-host parasite community dynamics. Trends Parasitol. 31, 212–221
Tylenchina
Rhabdida
Plecda
Orders
Inv_d
Spirurina
Suborders ae rcid oce r g a Cre
AgResearch, Ruakura Research Centre, Hamilton 3240, New Zealand 2 Centre for Parasitology of the A.N. Severtsov Institute of Ecology and Evolution, RAS 119071, Moscow, Russia
Inv_ip Inv_m
8. Spiridonov, S.E. (1989) New species of Rhigonematida (Nematoda) from the Cuban spirobolid Rhinocricus sp. (Diplopoda). Folia Parasitol. 36, 71–82 9. Dunn, A.M. and Hatcher, M.J. (2015) Parasites and biological invasions: parallels, interactions, and control. Trends Parasitol. 31, 189–199 10. Ross, J.L. et al. (2010) The role of parasite release in invasion of the USA by European slugs. Biol. Invas. 12, 603–610 11. Bedding, R.A. and Iede, E.T. (2005) Application of Beddingia siricidicola for Sirex woodwasp control. In Nematodes as Biocontrol Agents (Grewal, P.S. et al., eds), pp. 385–399, CABI Publishing 12. Fenton, A. et al. (2002) Optimal application strategies for entomopathogenic nematodes: integrating theoretical and empirical approaches. J. Appl. Ecol. 39, 481–492
Figure 1. Phylogenetic Relationships of Nematode Parasites of Invertebrates in the Orders Rhabditida and Plectida Showing Multiple Independent Acquisitions of Parasitism in Diplopods, Annelids, and Terrestrial Mollusks. Phylogenetic links of nematodes that parasitize vertebrates are also highlighted (*, probable common ancestor of such groups). Abbreviations: Inv_a, parasitism in annelid host; Inv_di, parasitism in insect and diplopod host; Inv_d, parasitism in diplopod host; Inv_i, parasitism in insects; Inv_ip, nematode pathogenic for insects (vectors of pathogenic bacteria); Inv_m, parasitism in mollusk host; In_mp, nematode pathogenic for mollusks; Vert, parasitism in vertebrates.
2
Trends in Parasitology, Month Year, Vol. xx, No. yy