The weird eusociality of polyembryonic parasites

0 2


1. The new eusocial systems

Eusociality is one of the most substantial guiding paradigms for social evolutionary research. Since its popularization in the mid-twentieth century [1], researchers across study taxa and disciplines have engaged in a shared evolutionary theory for how animals evolve overlapping generations, cooperative brood care and reproductive division of labour. Originally referring to certain species of Hymenoptera (e.g. ants, bees, wasps) and Isoptera (termites), the eusocial category has expanded to include species of aphids [2], thrips [3], shrimps [4], beetles [5] and naked mole rats [6]. Recently, however, larval colonies of trematodes (i.e. flatworms, blood flukes) are argued to be eusocial, following the discovery of morphologically distinct soldier castes [7], and this claim has received growing support [8–13]. This discovery is unexpected and exciting, extending our social evolutionary theories into a phylum (Platyhelminthes) that seemingly had no relevance to social evolution research. It is very confusing, therefore, that this phenomenon of soldier larvae in a parasitic colony has been known in polyembryonic wasps since 1981 [14], but is still often rejected as an example of eusociality [14–18], and even neglected from otherwise broad discussions of social evolution in wasps and Hymenoptera [19–23].

Polyembryonic wasps have been rejected from the category of eusociality because of their lack of overlapping parent–offspring generations, which is a requirement of the still popular sensu-Wilson definition [1]. New definitions for eusociality have been proposed by multiple authors since the 1990s, and virtually all of them pull importance away from overlapping generations, focusing more attention on comparing taxa by their reproductive divisions of labour [24–27]. Unfortunately, updating the deep terminology of social evolution research has been slow and controversial [28,29], and arguably no new consensus has been reached [30]. The eusocial status of polyembryonic wasps remained unique and uncertain until recently. Trematodes are also polyembryonic parasites with soldier castes in their larval colonies, but they technically do possess overlapping generations [31]. To consider only one of these systems as eusocial is confusing and contradictory—a case of semantics clouding comparative biology.

Overcoming this comparative confusion requires more than a terminological debate. Overlapping parent–offspring generations remain important because parental care (i.e. subsociality) is a firmly established prerequisite in evolutionary theories of sterile castes in animal societies [32,33]. Beyond semantics, how do we account for larval colonies of parasites that have converged upon sterile helper castes absent of the family-living context we observe in all other eusocial systems? Answering this is important, as polyembryonic parasites are useful exceptions to the eusocial norms receiving much attention from research on reproductive divisions of labour. Indeed, parasites are potentially full of undiscovered systems possessing behaviours convergent to social and eusocial taxa [34–37], and if we are going to include this incredibly common lifestyle in our social evolutionary theories, we can start by understanding the weird eusociality found in polyembryonic parasites.

2. Polyembryonic soldier castes do not require overlapping generations

Trematode and polyembryonic wasp species with soldier castes share similar life histories (figure 1) and selective pressures. In each case, an endoparasitic population originates from polyembryony, where a single egg splits into multiple embryos [38,43] and some of these embryos become morphologically and behaviourally distinct soldiers, improving the fitness of their colony by attacking competitors developing in the same host [44,45]. The single difference leading trematodes to be called eusocial, but not polyembryonic, wasps is that the first generation of trematode larvae descending from polyembryony continue to asexually produce new generations of larvae, while the polyembryonic wasp larvae do not (figure 1b,d). For these parasites, these overlapping generations only highlight differences in polyembryonic development. Unlike for the bees in which eusociality was first described [46], the presence or absence of overlapping generations in these parasites does not determine what brood care behaviours or reproductive divisions are capable of evolving. Importantly, ‘overlapping generations’ in most contexts refers to sexually mature stages of a life cycle spatially associated with offspring in earlier life stages, but this is never the case for polyembryonic parasites.

Figure 1. Life cycle and larval development in polyembryonic wasps and trematodes. (a) Polyembryonic wasps (e.g. Copidosoma floridanum [38,39]) lay one or more eggs into hosts, which develop into larvae and pupae while in this host. (b) The egg becomes a morula, splitting into polymorulae, which develop into sterile soldiers or regular larvae (i.e. ‘reproductive larvae’) that pupate and become sexually mature. All of these developmental stages are technically one generation (white bar). (c) Trematode (e.g. Himasthla rhigedana [40–42]) adults lay eggs which are released from their vertebrate hosts, find snails and multiply into a population of larvae. (d) Trematode eggs develop into a single sporocyst larva, which produces the first generation of rediae (i.e. larvae with mouths). It is unknown if soldier morphs are also produced in this first generation, but soldiers are certainly present in the daughter rediae generation, as well as cercariae—the dispersive morph. Multiple generations overlap during the daughter generations (grey shaded bar).

Trematodes are similar to the gall-forming aphids which can exhibit all the criteria of eusociality only during their asexual multiplication stage inside galls [2,21]. In trematodes and aphids, a multigenerational population can occur during these asexual life stages, allowing kin to specialize in caring for their developing siblings. In polyembryonic wasps, a ‘multi-developmental’ population occurs, where the polymorulae descending from the same zygote develop at different rates on different pathways [38,47], with soldiers developing before their siblings become larvae or pupae. This allows a caste system and brood caring relationship to form within one short-lived generation, absent of parents, as brood care for each other.

This quality of non-helpless brood is expected for parasite life cycles that use multiple hosts, or only use hosts for certain life stages, since each life stage might develop isolated from the previous one, effectively preventing direct care across generations. It is also the norm for some termites, aphids and other hemimetabolous social insects where the brood are precocial and perform tasks as juveniles [19,48–50]. Despite their differences, polyembryonic parasites have converged upon a hallmark of other eusocial taxa (soldier castes), and they do not represent an alternative explanation for eusociality. If we look past their lack of overlapping generations or traditional parental care, these polyembryonic groups fit surprisingly well into modern theories explaining eusociality in animal groups with overlapping generations.

3. Family living facilitates social evolution, but so does polyembryony

Why are overlapping generations important for the evolution of eusocial groups? While convincing arguments have been made for why we can ignore this trait in our terminological categories [25], parent–offspring grouping plays a fundamental role in the evolution of social behaviours via kin selection [51], and is incorporated into many theoretical frameworks of social evolution [52–56]. However, family living is not intrinsically important. It is the benefits and the consequences of family living that make it relevant to our evolutionary theories [57]. Family living is a proxy for more specific traits that facilitate social evolution, and polyembryonic groups achieve many of these same qualities (table 1). For instance, family groups and clonal groups achieve high relatedness facilitating the evolution of cooperative or altruistic behaviours following Hamilton’s rule [51]. The resilience and relevance of Hamilton’s theories have contributed to the popularity of the subsocial (i.e. fraternal) hypothesis for evolving eusociality [20,58,59], countering the alternative semi-social (i.e. egalitarian) hypothesis [54]. Interestingly, even controversial alternatives rejecting Hamilton’s rule [60] suggest group living inside a shared food source can substitute for a family living or kinship requirement. All endoparasites live inside their food source, and most, if not all, polyembryonic parasites are endoparasitic [17].

Table 1. Similarities and differences between social groups featuring parent–offspring overlap (i.e. family living) versus larval colonies descending from polyembryony.

characteristics family living polyembryony
spatial and temporal overlap of individuals ✓ yes, living in the same nest ✓ yes, living in the same host
high genetic relatedness ✓ 50, 75 or 100% related ✓ 100% related
variety of developmental stages ✓ yes, owing to production of multiple generations ✓ yes, owing to embryos developing at different rates (polyembryonic wasps) or larvae asexually reproducing (trematodes)
offspring help other offspring ✓ foraging for non-self, nest defence, reproductive sacrifice ✓ nest defence, reproductive sacrifice
offspring help developing young ✓ adults care for and/or defend brood ✓ brood defend brood, even within the same generation
offspring help parents ✓ adult offspring care for and/or defend mother × mother is absent; soldiers defend brood in her absence

An extension of the subsocial route to eusociality is the ‘lifetime monogamy’ hypothesis, which predicts that the ancestral state of all eusocial groups with obligate sterile helpers was once both subsocial and monogamous [55]. A central argument for the importance of this bottleneck origin is that the offspring of a monogamous pair are the closest a sexually produced group of animals can come to having a shared singular origin analogous to the zygotes of multicellular eukaryotic organisms. A polyembryonic colony is even more similar to this, being a group of animals literally descending from a single egg.

While these theories emphasize the role of kinship, others emphasize ecological conditions favouring sterile helper evolution. The ‘completely overlapping generations rule’ [33] suggests that obligately sterile helpers can only evolve if they can commit their entire lifetime to raising their parent’s brood. This commitment is made possible by living with a mother that lives longer than her offspring. In theory, a sterile helper can continue this commitment even if the mother is absent, as long as her brood persist and need care [33]. This is precisely the situation of polyembryonic parasites. For both trematodes and polyembryonic wasps, the mother of the polyembryonic egg is absent, but soldier morphs can spend their entire lives defending her offspring, never dispersing from their host. However, while polyembryonic wasps soldiers are sterile [38], the totipotency of trematode soldiers is not yet ruled out.

Polyembryonic parasites are consistent with core principles meant for explaining eusocial groups of parents living with adult offspring. They join other parasite taxa (aphids, thrips) as examples of ‘fortress-defender’ or ‘soldier-first’ eusociality, in which a primary function of the non-reproducing caste is nest defence, rather than foraging, feeding or housekeeping [15,19,50]. For this reason, it makes sense that authors do not include polyembryonic wasps in reviews of hymenopteran sociality [20–23], as virtually all ants, bees and wasps fit a ‘life-insurer’ or ‘worker-first’ pathway to eusociality [15,19], and parasitoid wasps are phylogenetically distinct from other social wasps.

4. Where do the polyembryonic parasites fit in?

Fortunately, researchers of polyembryonic wasps are aware of their similarities to eusocial taxa, and study topics such as caste determination [38,60], caste allocation [61,62], nest-mate recognition [63,64] and even sex-ratio conflict like in other Hymenoptera [65–67]. While some authors claim they are eusocial [25,68,69], others avoid explicit attribution of eusociality to polyembryonic wasps [8,41,60–62,67,70–72], or clearly state they are not eusocial [14–17] (electronic supplementary material, table S1). I urge authors to not feel pressured to fit their system into the sensu-Wilson definition [1], for they can cite the sensu-Crespi definition [25], and/or refer to them as fortress defenders [19,50], as this term was inspired by the discovery of parasites with soldier castes. The contributions from polyembryonic wasps to the evolution of reproductive division of labour are not invalidated by their lack of overlapping generations, and this character requirement was only popularized as an initial demarcation to guide, not blind, our search for eusociality across taxa [1].

How we categorize and compare eusociality in polyembryonic wasps and trematodes will change as we learn more about each system, and incorporate other instances of polyembryony and parasitism featuring divisions of labour [73]. Cnidarians and bryozoans are both polyembryonic, but can exhibit division of labour among their polyps and zooids separate from a parasitic context [74,75]. Additionally, while defence against competitors or predators is a common function of polyembryonic castes, it is not their only function (e.g. nutrient transfer in bryozoans [76], sex-ratio optimization in polyembryonic wasps [65,66]). At the moment, trematodes might be the only taxon without a clear alternative function for their soldier castes. Hypotheses on their caste evolution can be informed with the continued research on sociality in trematodes, and a better understanding of their phylogenetic relationships. For instance, trematode species exhibiting a specialized role of the first reproductive larva [77] could be viewed as a eusocial precursor, analogous to the dwarf eldest daughter in carpenter bees [78], depending on how we build our phylogenies.

Parasitism, regardless of polyembryony, can facilitate the coincidence of food, shelter and group living [35,50], which are factors relevant to social evolution in all taxa. Unique to parasitism and other host–symbiont relationships, though, is the potential influence of the host on social evolution. In aphids and thrips, soldiers are associated with host plants that prolong gall formation [21,79], but comparable metrics are not yet supported in polyembryonic wasps or trematodes. In theory, when parasite niches overlap, the fitness benefits of aggressive interference (and thus soldier morphs) should positively correlate with host characteristics that increase susceptibility (or exposure [13]) to parasite co-infections. We will learn more about the selective conditions favouring soldier castes with further understanding of parasite competitive ecology, which, serendipitously, is also a potentially useful avenue of research for medically relevant parasitology [80,81].

Beyond comparing competitive contexts, the developmental biology of these parasites is also necessary for understanding soldier caste evolution. The detailed ontogeny of polyembryonic wasps shows how the sterility of soldier morphs is determined early in development [38], but a similar depth of caste determination has yet to be described in trematode species with soldier castes.

5. Conclusion

Both trematodes and polyembryonic wasps possessing soldier castes can be considered eusocial, regardless of an overlapping generations criterion. Polyembryonic parasites have many differences from parent–offspring groups, but also possess many similarities that facilitate the convergent evolution of social behaviours and sterile castes. Polyembryonic parasites support the bottleneck origin of the lifetime monogamy hypothesis [55], meet the special exceptions to the completely overlapping generations rule for evolving sterile castes [33], and are more comparable to a subsocial than the semi-social route to eusociality [54]. This highlights how important relatedness and ecological conditions are for social evolutionary explanations in any system. While trematodes possess overlapping generations of larvae, and polyembryonic wasps do not, at the moment this only amounts to a difference in polyembryonic development and caste determination.

Acknowledging the eusociality of polyembryonic parasites will build a constructive conversation around the special case of polyembryony for major evolutionary transitions theories [53,82]. An egg developing on a path towards one multicellular body, eventually splitting into multiple multicellular bodies, provides unique challenges to our concepts of biological individuality. For instance, a group of polyembryonic parasites could be considered a ‘modular organism’ [18], like clonal plants or siphonophores. However, polyembryonic wasps separate germ and soma early on during embryogenesis, and the soma never exhibits modular reproduction, as occurs in other modular organisms [38]. In fact, the caste determination mechanism of polyembryonic wasps is perhaps their most fascinating contribution. Soldiers are polymorulae that never receive germinal cells [17,38]. Their separation of castes is not functionally similar to a multicellular germ/soma separation: it is literally the same mechanism of embryogenic cell differentiation. For this reason, polyembryonic wasps represent one of the greatest empirical confirmations of major evolutionary transitions theory, and the universal nature of social evolutionary principles across levels of biological organization.

Competing interests

I declare I have no competing interests.

Funding

I received funding from the Edna and Yoshinori ‘Joe’ Tanada Endowed Fellowship and the Julius H. Freitag Memorial Award.

Acknowledgements

I would like to thank the anonymous reviewers of this manuscript, as well as Dr Eileen Lacey, Dr Neil Tsutsui, Wenjing Xu, Jessica Maccaro and Sean Perez, for helpful comments and discussions that shaped my perspective, and Dr Ana Garcia-Vedrenne and Dr Ryan Hechinger for introducing me to the social trematodes of California.

Footnotes

Electronic supplementary material is available online at https://doi.org/10.6084/m9.figshare.c.5354877.

© 2021 The Authors.

Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

References

  • 1.
    Wilson EO. 1971The insect societies. Cambridge, MA: Harvard University Press. Google Scholar

  • 2.
    Aoki S. 1977Colophina clematis (Homoptera, Pemphigidae), and aphid species with ‘soldiers’. 昆蟲 45, 276-282. Google Scholar

  • 3.
    Crespi BJ. 1992Eusociality in Australian gall thrips. Nature 359, 724-726. (doi:10.1038/359724a0) Crossref, ISI, Google Scholar

  • 4.
    Duffy JE. 1996Eusociality in a coral-reef shrimp. Nature 381, 512-514. (doi:10.1038/381512a0) Crossref, ISI, Google Scholar

  • 5.
    Kent DS, Simpson JA. 1992Eusociality in the beetle Austroplatypus incompertus (Coleoptera: Curculionidae). Naturwissenschaften 79, 86-87. (doi:10.1007/BF01131810) Crossref, Google Scholar

  • 6.
    Jarvis JUM. 1981Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science 212, 571-573. (doi:10.1126/science.7209555) Crossref, PubMed, ISI, Google Scholar

  • 7.
    Hechinger RF, Wood AC, Kuris AM. 2011Social organization in a flatworm: trematode parasites form soldier and reproductive castes. Proc. R. Soc. B 278, 656-665. (doi:10.1098/rspb.2010.1753) Link, ISI, Google Scholar

  • 8.
    Newey P, Keller L. 2010Social evolution: war of the worms. Curr. Biol. 20, 985-987. (doi:10.1016/j.cub.2010.10.010) Crossref, ISI, Google Scholar

  • 9.
    Miura O. 2012Social organization and caste formation in three additional parasitic flatworm species. Mar. Ecol. Prog. Ser. 465, 119-127. (doi:10.3354/meps09886) Crossref, ISI, Google Scholar

  • 10.
    Garcia-Vedrenne AE, Quintana ACEE, Derogatis AM, Martyn K, Kuris AM, Hechinger RF. 2016Social organization in parasitic flatworms—four additional echinostomoid trematodes have a soldier caste and one does not. J. Parasitol. 102, 11-20. (doi:10.1645/15-853) Crossref, PubMed, ISI, Google Scholar

  • 11.
    Garcia-Vedrenne AE, Quintana ACE, DeRogatis AM, Dover CM, Lopez M, Kuris AM, Hechinger RF. 2017Trematodes with a reproductive division of labour: heterophyids also have a soldier caste and early infections reveal how colonies become structured. Int. J. Parasitol. 47, 41-50. (doi:10.1016/j.ijpara.2016.10.003) Crossref, PubMed, ISI, Google Scholar

  • 12.
    Poulin R, Kamiya T, Lagrue C. 2019Evolution, phylogenetic distribution and functional ecology of division of labour in trematodes. Parasites Vectors 12, 5. (doi:10.1186/s13071-018-3241-6) Crossref, PubMed, ISI, Google Scholar

  • 13.
    Resetarits EJ, Torchin ME, Hechinger RF. 2020Social trematode parasites increase standing army size in areas of greater invasion threat. Biol. Lett. 16, 20190765. (doi:10.1098/rsbl.2019.0765) Link, ISI, Google Scholar

  • 14.
    Cruz YP. 1981A sterile defender morph in a polyembryonic hymenopterous parasite. Nature 294, 446-447. (doi:10.1038/294446a0) Crossref, ISI, Google Scholar

  • 15.
    Tian L, Zhou X. 2014The soldiers in societies: defence, regulation, and evolution. Int. J. Biol. Sci. 10, 296-308. (doi:10.7150/ijbs.6847) Crossref, PubMed, ISI, Google Scholar

  • 16.
    Ode PJ, Keasar T, Segoli M. 2018Lessons from the multitudes: insights from polyembryonic wasps for behavioral ecology. Curr. Opin. Insect Sci. 27, 32-37. (doi:10.1016/j.cois.2018.02.001) Crossref, PubMed, ISI, Google Scholar

  • 17.
    Iwabuchi K. 2019Polyembryonic insects. Singapore: Springer. (doi:10.1007/978-981-15-0958-2) Crossref, Google Scholar

  • 18.
    Boomsma JJ, Gawne R. 2018Superorganismality and caste differentiation as points of no return: how the major evolutionary transitions were lost in translation. Biol. Rev. 93, 28-54. (doi:10.1111/brv.12330) Crossref, PubMed, ISI, Google Scholar

  • 19.
    Queller DC, Strassmann JE. 1998Kin selection and social insects. Bioscience 48, 165-175. (doi:10.2307/1313262) Crossref, ISI, Google Scholar

  • 20.
    Rehan SM, Toth AL. 2015Climbing the social ladder: the molecular evolution of sociality. Trends Ecol. Evol. 30, 426-433. (doi:10.1016/j.tree.2015.05.004) Crossref, PubMed, ISI, Google Scholar

  • 21.
    Rubenstein DR, Abbot P. 2017Comparative social evolution. Cambridge, MA: Harvard University Press. (doi:10.1017/9781107338319) Crossref, Google Scholar

  • 22.
    Taylor D, Bentley MA, Sumner S. 2018Social wasps as models to study the major evolutionary transition to superorganismality. Curr. Opin. Insect Sci. 28, 26-32. (doi:10.1016/j.cois.2018.04.003) Crossref, PubMed, ISI, Google Scholar

  • 23.
    Linksvayer TA, Johnson BR. 2019Re-thinking the social ladder approach for elucidating the evolution and molecular basis of insect societies. Curr. Opin. Insect Sci. 34, 123-129. (doi:10.1016/j.cois.2019.07.003) Crossref, PubMed, ISI, Google Scholar

  • 24.
    Gadagkar R. 1994Why the definition of eusociality is not helpful to understand its evolution and what should we do about it. Oikos 70, 485. (doi:10.2307/3545789) Crossref, ISI, Google Scholar

  • 25.
    Crespi BJ, Yanega D. 1995The definition of eusociality. Behav. Ecol. 6, 109-115. (doi:10.1093/beheco/6.1.109) Crossref, ISI, Google Scholar

  • 26.
    Sherman PW, Lacey EA, Reeve HK, Keller L. 1995The eusociality continuum. Behav. Ecol. 6, 102-108. (doi:10.1093/beheco/6.1.102) Crossref, ISI, Google Scholar

  • 27.
    Rubenstein DR, Botero CA, Lacey EA. 2016Discrete but variable structure of animal societies leads to the false perception of a social continuum. R. Soc. Open Sci. 3, 160147. (doi:10.1098/rsos.160147) Link, ISI, Google Scholar

  • 28.
    Wcislo WT. 1997Are behavioral classifications blinders to studying natural variation? In The evolution of social behaviour in insects and arachnids (eds Choe J, Crespi B), pp. 8-13. Cambridge, UK: Cambridge University Press. (doi:10.1017/cbo9780511721953.002) Crossref, Google Scholar

  • 29.
    Costa JT, Fitzgerald TD. 1996Developments in social terminology: semantic battles in a conceptual war. Trends Ecol. Evol. 11, 285-289. (doi:10.1016/0169-5347(96)10035-5) Crossref, PubMed, ISI, Google Scholar

  • 30.
    Costa JT. 2018The other insect societies: overview and new directions. Curr. Opin. Insect Sci. 28, 40-49. (doi:10.1016/j.cois.2018.04.008) Crossref, PubMed, ISI, Google Scholar

  • 31.
    Maule AG, Marks NJ. 2006Parasitic flatworms: molecular biology, biochemistry, immunology and physiology. Wallingford, UK: CABI Publishing. (doi:10.1079/9780851990279.0000) Google Scholar

  • 32.
    Toth AL, Rehan SM. 2017Molecular evolution of insect sociality: an eco-evo-devo perspective. Annu. Rev. Entomol. 62, 419-442. (doi:10.1146/annurev-ento-031616-035601) Crossref, PubMed, ISI, Google Scholar

  • 33.
    Downing PA, Cornwallis CK, Griffin AS. 2017How to make a sterile helper. Bioessays 39, e201600136. (doi:10.1002/bies.201600136) Crossref, ISI, Google Scholar

  • 34.
    Wickler W. 1976Evolution-oriented ethology, kin selection, and altruistic parasites. Z. Tierpsychol. 42, 206-214. (doi:10.1111/j.1439-0310.1976.tb00966.x) Crossref, PubMed, Google Scholar

  • 35.
    Lopez MA, Nguyen HT, Oberholzer M, Hill KL. 2011Social parasites. Curr. Opin. Microbiol. 14, 642-648. (doi:10.1016/j.mib.2011.09.012) Crossref, PubMed, ISI, Google Scholar

  • 36.
    Crespi BJ. 2001The evolution of social behavior in microorganisms. Trends Ecol. Evol. 16, 178-183. (doi:10.1016/S0169-5347(01)02115-2) Crossref, PubMed, ISI, Google Scholar

  • 37.
    Secor PR, Dandekar AA. 2020More than simple parasites: the sociobiology of bacteriophages and their bacterial hosts. MBio 11, e00041-20. (doi:10.1128/mBio.00041-20) Crossref, PubMed, ISI, Google Scholar

  • 38.
    Strand MR. 2009Polyembryony. In Encyclopedia of insects, 2nd edn (eds Resh VH, Cardé RT), pp. 821-825. Burlington, MA: Elsevier. (doi:10.1016/B978-0-12-374144-8.00217-4) Crossref, Google Scholar

  • 39.
    Grbic M, Rivers D, Strand MR. 1997Caste formation in the polyembryonic wasp Copidosoma floridanum (Hymenoptera: Encyrtidae): in vivo and in vitro analysis. J. Insect Physiol. 43, 553-565. (doi:10.1016/S0022-1910(97)00004-8) Crossref, PubMed, ISI, Google Scholar

  • 40.
    Adams JE, Martin WE. 1963Life cycle of Himasthla rhigedana Dietz, 1909 (Trematoda: Echinostomatidae). Source Trans. Am. Microsc. Soc. 82. Google Scholar

  • 41.
    Erasmus DA. 1972The biology of trematodes. London, UK: Edward Arnold. Google Scholar

  • 42.
    Hechinger RF. 2019Guide to the trematodes (Platyhelminthes) that infect the California horn snail (Cerithideopsis californica: Potamididae: Gastropoda) as first intermediate host. Zootaxa 4711, 459-494. (doi:10.11646/zootaxa.4711.3.3) Crossref, ISI, Google Scholar

  • 43.
    Esch GW. 2002The transmission of digenetic trematodes: style, elegance, complexity. Integr. Comp. Biol. 42, 304-312. (doi:10.1093/icb/42.2.304) Crossref, PubMed, ISI, Google Scholar

  • 44.
    Lloyd MM, Poulin R. 2012Fitness benefits of a division of labour in parasitic trematode colonies with and without competition. Int. J. Parasitol. 42, 939-946. (doi:10.1016/j.ijpara.2012.07.010) Crossref, PubMed, ISI, Google Scholar

  • 45.
    Giron D, Ross KG, Strand MR. 2007Presence of soldier larvae determines the outcome of competition in a polyembryonic wasp. J. Evol. Biol. 20, 165-172. (doi:10.1111/j.1420-9101.2006.01212.x) Crossref, PubMed, ISI, Google Scholar

  • 46.
    Batra S. 1966Nests and social behavior of halictine bees of India (Hymenoptera: Halictidae). Indian J. Entomol. 28, 375-393. Google Scholar

  • 47.
    Cruz YP, Oelhaf RC, Jockusch EL. 1990Polymorphic precocious larvae in the polyembryonic parasitoid Copidosomopsis tanytmema (Hymenoptera: Encyrtidae). Ann. Entomol. Soc. Am. 83, 549-554. (doi:10.1093/aesa/83.3.549) Crossref, ISI, Google Scholar

  • 48.
    Howard KJ, Thorne BL. 2011Eusocial evolution in termites and hymenoptera. In Biology of termites: a modern synthesis (eds Bignell D, Roisin Y, Lo N), pp. 97-132. Dordrecht, The Netherlands: Springer. (doi:10.1007/978-90-481-3977-4_5) Google Scholar

  • 49.
    Costa J. 2006The other insect societies. Cambridge, MA: Harvard University Press. (doi:10.5860/choice.44-6237) Google Scholar

  • 50.
    Crespi BJ. 1994Three conditions for the evolution of eusociality: are they sufficient?Insectes Sociaux 41, 395-400. (doi:10.1007/BF01240642) Crossref, ISI, Google Scholar

  • 51.
    Hamilton WD. 1964The genetical evolution of social behaviour. II. J. Theor. Biol. 7, 17-52. (doi:10.1016/0022-5193(64)90039-6) Crossref, PubMed, ISI, Google Scholar

  • 52.
    Alexander R. 1974The evolution of social life. Annu. Rev. Ecol. Syst. 5, 325-383. (doi:10.1146/annurev.es.05.110174.001545) Crossref, Google Scholar

  • 53.
    Maynard Smith J, Szathmary E. 1997The major transitions in evolution. Oxford, UK: Oxford University Press. (doi:10.1093/oso/9780198502944.001.0001) Crossref, Google Scholar

  • 54.
    Bourke AFG. 2011Principles of social evolution. Oxford, UK: Oxford University Press. (doi:10.1093/acprof:oso/9780199231157.001.0001) Crossref, Google Scholar

  • 55.
    Boomsma JJ. 2009Lifetime monogamy and the evolution of eusociality. Phil. Trans. R. Soc. B 364, 3191-3207. (doi:10.1098/rstb.2009.0101) Link, ISI, Google Scholar

  • 56.
    Socias-Martínez L, Kappeler PM. 2019Catalyzing transitions to sociality: ecology builds on parental care. Front. Ecol. Evol. 7, 160. (doi:10.3389/fevo.2019.00160) Crossref, ISI, Google Scholar

  • 57.
    Kramer J, Meunier J. 2019The other facets of family life and their role in the evolution of animal sociality. Biol. Rev. 94, 199-215. (doi:10.1111/brv.12443) Crossref, ISI, Google Scholar

  • 58.
    Queller DC. 2000Relatedness and the fraternal major transitions. Phil. Trans. R. Soc. Lond. B 355, 1647-1655. (doi:10.1098/rstb.2000.0727) Link, ISI, Google Scholar

  • 59.
    Linksvayer TA. 2019Subsociality and the evolution of eusociality. In Encyclopedia of animal behavior (eds Breed MD, Moore J), pp. 661-666. Elsevier. (doi:10.1016/B978-0-12-809633-8.20847-9) Crossref, Google Scholar

  • 60.
    Nowak MA, Tarnita CE, Wilson EO. 2010The evolution of eusociality. Nature 466, 1057-1062. (doi:10.1038/nature09205) Crossref, PubMed, ISI, Google Scholar

  • 61.
    Harvey JA, Corley LS, Strand MR. 2000Competition induces adaptive shifts in caste ratios of a polyembryonic wasp. Nature 406, 183-186. (doi:10.1038/35018074) Crossref, PubMed, ISI, Google Scholar

  • 62.
    Watanabe K, Nishide Y, Roff DA, Yoshimura J, Iwabuchi K. 2012Environmental and genetic controls of soldier caste in a parasitic social wasp. Scient. Rep. 2, 729. (doi:10.1038/srep00729) Crossref, PubMed, ISI, Google Scholar

  • 63.
    Giron D, Strand MR. 2004Host resistance and the evolution of kin recognition in polyembryonic wasps. Proc. R. Soc. Lond. B 271, 395-398. (doi:10.1098/rsbl.2004.0205) Link, ISI, Google Scholar

  • 64.
    Giron D, Dunn DW, Hardy ICW, Strand MR. 2004Aggression by polyembryonic wasp soldiers correlates with kinship but not resource competition. Nature 430, 676-679. (doi:10.1038/nature02721) Crossref, PubMed, ISI, Google Scholar

  • 65.
    Grbić M, Ode PJ, Strand MR. 1992Sibling rivalry and brood sex ratios in polyembryonic wasps. Nature 360, 254-256. (doi:10.1038/360254a0) Crossref, ISI, Google Scholar

  • 66.
    Gardner A, Hardy ICW, Taylor PD, West SA. 2007Spiteful soldiers and sex ratio conflict in polyembryonic parasitoid wasps. Am. Nat. 169, 519-533. (doi:10.1086/512107) Crossref, PubMed, ISI, Google Scholar

  • 67.
    Rautiala P, Gardner A. 2016Intragenomic conflict over soldier allocation in polyembryonic parasitoid wasps. Am. Nat. 187, E106-E115. (doi:10.1086/685082) Crossref, PubMed, ISI, Google Scholar

  • 68.
    Nishide Y, Watanabe K, Inoue H, Moriyama H, Satoh T, Hinomoto N, Iwabuchi K. 2013Isolation of novel microsatellite markers for the social parasitoid wasp, Copidosoma floridanum (Hymenoptera: Encyrtidae). Appl. Entomol. Zool. 48, 93-96. (doi:10.1007/s13355-012-0144-4) Crossref, ISI, Google Scholar

  • 69.
    Carmel Y, Shavit A. 2020Operationalizing evolutionary transitions in individuality. Proc. R. Soc. B 287, 20192805. (doi:10.1098/rspb.2019.2805) Link, ISI, Google Scholar

  • 70.
    Zhurov V, Terzin T, Grbić M. 2004Early blastomere determines embryo proliferation and caste fate in a polyembryonic wasp. Nature 432, 764-769. (doi:10.1038/nature03171) Crossref, PubMed, ISI, Google Scholar

  • 71.
    Segoli M, Harari AR, Rosenheim JA, Bouskila A, Keasar T. 2010The evolution of polyembryony in parasitoid wasps. J. Evol. Biol. 23, 1807-1819. (doi:10.1111/j.1420-9101.2010.02049.x) Crossref, PubMed, ISI, Google Scholar

  • 72.
    Otsuki Tet al.2019Mass killing by female soldier larvae is adaptive for the killed male larvae in a polyembryonic wasp. Scient. Rep. 9, 7357. (doi:10.1038/s41598-019-43643-3) Crossref, PubMed, ISI, Google Scholar

  • 73.
    Craig SF, Slobodkin LB, Wray GA, Biermann CH. 1997The ‘paradox’ of polyembryony: a review of the cases and a hypothesis for its evolution. Evol. Ecol. 11, 127-143. (doi:10.1023/A:1018443714917) Crossref, ISI, Google Scholar

  • 74.
    Ayre DJ, Grosberg RK. 2005Behind anemone lines: factors affecting division of labour in the social cnidarian Anthopleura elegantissima. Anim. Behav. 70, 97-110. (doi:10.1016/j.anbehav.2004.08.022) Crossref, ISI, Google Scholar

  • 75.
    Lidgard S, Carter MC, Dick MH, Gordon DP, Ostrovsky AN. 2012Division of labor and recurrent evolution of polymorphisms in a group of colonial animals. Evol. Ecol. 26, 233-257. (doi:10.1007/s10682-011-9513-7) Crossref, ISI, Google Scholar

  • 76.
    Jenkins HL, Waeschenbach A, Okamura B, Hughes RN, Bishop JDD. 2017Phylogenetically widespread polyembryony in cyclostome bryozoans and the protracted asynchronous release of clonal brood-mates. PLoS ONE 12, e0170010. (doi:10.1371/journal.pone.0170010) Crossref, PubMed, ISI, Google Scholar

  • 77.
    Sapp KK, Meyer KA, Loker ES. 1998Intramolluscan development of the digenean Echinostoma paraensei: rapid production of a unique mother redia that adversely affects development of conspecific parasites. Invertebr. Biol. 117, 20. (doi:10.2307/3226848) Crossref, ISI, Google Scholar

  • 78.
    Rehan SM, Berens AJ, Toth AL. 2014At the brink of eusociality: transcriptomic correlates of worker behaviour in a small carpenter bee. BMC Evol. Biol. 14, 260. (doi:10.1186/s12862-014-0260-6) Crossref, PubMed, ISI, Google Scholar

  • 79.
    Pike N, Whitfield JA, Foster WA. 2007Ecological correlates of sociality in Pemphigus aphids, with a partial phylogeny of the genus. BMC Evol. Biol. 7, 185. (doi:10.1186/1471-2148-7-185) Crossref, PubMed, ISI, Google Scholar

  • 80.
    Mideo N. 2009Parasite adaptations to within-host competition. Trends Parasitol. 25, 261-268. (doi:10.1016/j.pt.2009.03.001) Crossref, PubMed, ISI, Google Scholar

  • 81.
    Laidemitt MR, Anderson LC, Wearing HJ, Mutuku MW, Mkoji GM, Loker ES. 2019Antagonism between parasites within snail hosts impacts the transmission of human schistosomiasis. eLife 8, e50095. (doi:10.7554/eLife.50095) Crossref, PubMed, ISI, Google Scholar

  • 82.
    West SA, Fisher RM, Gardner A, Kiers ET. 2015Major evolutionary transitions in individuality. Proc. Natl Acad. Sci. USA 112, 10 112-10 119. (doi:10.1073/pnas.1421402112) Crossref, ISI, Google Scholar

También podría gustarte
Deja una respuesta

Su dirección de correo electrónico no será publicada.

This website uses cookies to improve your experience. We'll assume you're ok with this, but you can opt-out if you wish. Accept Read More