Advertisement

The evolution of caste-biasing symbionts in the social hymenoptera

  • D. Treanor
  • T. Pamminger
  • W. O. H. Hughes
Open Access
Review Article

Abstract

The separation of individuals into reproductive and worker castes is the defining feature of insect societies. However, caste determination is itself a complex phenomenon, dependent on interacting genetic and environmental factors. It has been suggested by some authors that widespread maternally transmitted symbionts such as Wolbachia may be selected to interfere with caste determination, whilst others have discounted this possibility on theoretical grounds. We argue that there are in fact three distinct evolutionary scenarios in which maternally transmitted symbionts might be selected to influence the process of caste determination in a social hymenopteran host. Each of these scenarios generate testable predictions which we outline here. Given the increasing recognition of the complexity and multi-faceted nature of caste determination in social insects, we argue that maternally transmitted symbionts should also be considered as possible factors influencing the development of social hymenopterans.

Keywords

Social insects Symbiosis Caste determination Wolbachia 

Introduction

The defining feature of eusociality is reproductive division of labor (Oster and Wilson 1979; Crespi and Yanega 1995). Within a colony, individuals of different castes specialize in either reproduction (i.e., queens) or parental care and foraging (i.e., workers), and in many social insects, in particular the social hymenoptera, these behavioral castes also exhibit irreversible morphological differentiation (Wilson 1971). As a consequence, social insect colonies have to produce a mixture of new reproductives and workers from offspring of the same sex, and a major theme of research in social insect biology concerns the developmental processes underlying this. Until relatively recently, the prevailing view was that the development of totipotent larvae into either reproductives or workers was determined largely or entirely by environmental effects, but a number of studies have now shown effects of genotype on caste determination across a range of social insects (Anderson et al. 2008; Schwander et al. 2010). In some species these genetic effects are plastic, with individuals of certain genotypes displaying a moderate propensity towards developing into either reproductives or workers (Hughes and Boomsma 2007, 2008; Schwander and Keller 2008) whilst in other species, caste is determined almost entirely by genotype (Julian et al. 2002; Fournier et al. 2005; Darras et al. 2014; Kuhn et al. 2018).

Here, we discuss how natural selection may cause maternally transmitted symbionts (MTSs) to influence caste determination in the social hymenoptera. Heritable symbionts are extremely widespread in insects and vary enormously in terms of their effects on host organisms (Moran et al. 2008; Weinert et al. 2015). Some symbionts, such as Buchnera in aphids, are obligate mutualists of their hosts, providing essential metabolic functions (Shigenobu et al. 2000), whilst others enhance host fitness without being essential for survival (Oliver et al. 2003; Scarborough et al. 2005). Nevertheless, many MTSs have fundamentally selfish interests that differ from their hosts, because they can only be transmitted by females (Engelstädter and Hurst 2009a, b; Duron and Hurst 2013; Bennett and Moran 2015; Hurst and Frost 2015). This simple fact has led to the evolution of a profusion of manipulative traits in MTSs that increase the production of female offspring by infected hosts (Werren et al. 2008).

Heritable symbionts appear to be just as common in the social hymenoptera as they are in insects generally; numerous studies have reported the presence of complex symbiotic communities in ants, including taxa known to manipulate host reproduction (Wenseleers et al. 1998; Russell et al. 2009, 2012; Kautz et al. 2013), and such reproductive parasites have also been detected in social bees and wasps, as well as their solitary cousins (Evison et al. 2012; Gerth et al. 2013, 2015; de Oliveira et al. 2015). However, in the social hymenoptera, reproductive manipulation by MTSs may also extend to caste determination; only individuals of the reproductive caste are capable of propagating MTSs, and so these symbionts have a strong evolutionary interest in ensuring that first, they preferentially infect queens, and second, that their hosts preferentially produce queens.

Three distinct selective pressures can lead to the evolution of caste-biasing by symbionts

Bourke and Ratnieks (1999) suggested that MTSs such as Wolbachia might be party to social conflicts concerning caste determination in insect societies. They argued that, because symbionts such as Wolbachia cannot be transmitted through sterile workers, symbionts should evolve to manipulate the development of females so that they are more likely to develop into queens. These queens will then be capable of transmitting the infection to the next generation. On the other hand, Wenseleers (2001) argued that, since all females in a colony are clonally related from the perspective of an MTS, the MTS will be selected to mutualistically maximize colony productivity rather than bias the caste fate of developing larvae.

Whilst this logic is sound, it rests on three important assumptions: (1) that the fidelity of transmission of the symbiont from parent to offspring is perfect, i.e., infected queens produce only infected offspring; (2) that only a single maternal lineage is present within a colony; (3) that any symbiont present has no interest in distorting the sex ratio of its host. In reality, each of these assumptions is violated in nature and each creates a different arena for conflict over caste determination between MTSs and social hymenopteran hosts. Here, we discuss each of these scenarios in turn and describe how they might be experimentally investigated.

Caste-biasing due to imperfect vertical transmission of symbionts

In many instances, the fidelity of transmission of MTSs to the offspring of their host is impressively high, and essentially all the offspring of an infected female are themselves infected (e.g., Shoemaker et al. 2003). Nonetheless, there are many cases in which the fidelity of transmission of MTSs is less than perfect; in other words, infected females produce some uninfected offspring (Hoffmann et al. 1990; Hurst et al. 2001; Wenseleers et al. 2002; Graham and Wilson 2012; Oliver et al. 2014; Dykstra et al. 2014), despite the fact that ensuring a high transmission rate is clearly in the evolutionary interests of MTSs. In solitary insects, MTSs will be under selection to maximize their transmission to the female offspring of their host, because only female offspring are capable of propagating the symbiont. However, in many of the social hymenoptera, only queens can reproduce, and workers are either completely sterile or only capable of producing male offspring. As such, in social hymenopterans, MTSs will be subject to selection to maximize the infection rate of queens, rather than females generally. We suggest that an MTS infecting a social hymenopteran could maximize the infection rate of queens by increasing the likelihood that infected female offspring develop into queens rather than workers. In a simple scenario, a caste-biasing MTS might alter larval begging or feeding behavior, lengthen the developmental period of larvae, or reduce the effect of queen pheromones that inhibit the development of female larvae into new queens.

In a more sophisticated scenario, the MTS itself could become an additional caste-determining locus, being necessary but not sufficient for the development of female larvae into reproductives. MTSs might interfere with caste determination at a molecular level, perhaps even becoming an essential part of signaling pathways that lead to the development of larvae into queens. Such fundamental effects of MTSs on host biology are not without precedent; in some lineages of the isopod crustacean Armadillidium vulgare, Wolbachia has become the sex-determining locus, supplanting nuclear sex determination (Cordaux et al. 2011). An alternative mechanism might involve a parallel with the Medea phenotype found in Trilobium beetles. When a female has a copy of the gene medea, any of her offspring that fail to inherit a copy die as zygotes. Thus, the medea gene ensures that all the offspring produced by a female contain copies of itself (Beeman et al. 1992). Werren and O’Neill (1997) suggested that MTSs are likely to cause similar phenotypes, in which uninfected offspring of infected hosts will die or suffer reduced fitness. An equivalent situation could occur with regard to the caste fate of larvae. Instead of an MTS causing mortality in offspring that do not inherit it, it would cause uninfected offspring to develop into workers instead of queens.

A clear prediction of this hypothesis is that in species with a caste-biasing MTS, the prevalence of infection will be lower in the worker caste than in queens. Interestingly, this pattern has been observed for Wolbachia infection in a number of social insect species (Keller et al. 2001; Van Borm et al. 2001; Wenseleers et al. 2002; Frost et al. 2010; Roy et al. 2015). In the past, this has been attributed to other causes—in particular the proposed adaptive loss of infection from the worker caste (Keller et al. 2001; Wenseleers et al. 2002). Just as an MTS may be selected to preferentially infect the queen caste, if they impose a fitness cost upon their hosts, it follows that they will be selected to reduce their transmission to sterile workers. In this case, the interests of the MTS and the host colony will be aligned, as the host will also benefit from the reduced burden of infection in the worker caste (Wenseleers et al. 2002). Other explanations for reduced infection rates in the worker caste include ovarial regression in workers, or age-dependent changes in symbiont titers (Keller et al. 2001; Wenseleers et al. 2002; Russell 2012), but such relationships could alternatively be explained by the presence of a caste-biasing MTS with imperfect vertical transmission. These alternative hypotheses could be distinguished by examining the relative infection rates of larvae, queens, and workers (see Table 1.) Furthermore, it has recently been shown that Wolbachia infection in Aedes aegypti mosquitoes can be determined non-lethally using near-infrared spectroscopy (Sikulu-Lord et al. 2016). If applied to social hymenopterans, this would allow the developmental fate of larvae of known infection status to be tracked, providing a means of directly testing for the presence of a caste-biasing MTS.

Table 1

Examining the relative infection rates of larvae, queens, and workers provides a means of testing for caste-biasing MTSs, and distinguishing these from other causes of relatively low MTS infection rates in workers

Larval infection rate

Queen infection rate

Worker infection rate

Explanation

\(x\)

\(x\)

\(x\)

No adaptive loss or caste-biasing

\(x\)

\(x\)

\(<x\)

Adaptive loss, ovarial regression or age-dependent changes in symbiont titer in the worker caste

\(x\)

\(>x\)

\(< x\,{\text{or}}\, \sim x\)

Caste-biasing MTS

Caste-biasing due to the coexistence of multiple maternal lineages

In insect societies, genetic conflict over queen rearing occurs under two circumstances (Ratnieks et al. 2006). Firstly, queens of some species mate with multiple males, and this creates potential conflict between patrilines over queen rearing, as genes which increase the propensity of larvae to develop into sexual offspring may spread despite the probable colony-level cost of over-producing new queens; accordingly, patrilines which are overrepresented in sexual offspring have been identified in the honeybee Apis mellifera and the ant Acromyrmex echinatior (Moritz et al. 2005; Hughes and Boomsma 2008). Secondly, the presence of multiple matrilines within a colony also generates conflict over queen rearing. There are numerous examples of social hymenopterans with polygynous colonies formed of unrelated queens (Stille and Stille 1992; Evans 1996; Carew et al. 1997; Heinze and Keller 2000; Brown et al. 2003; Hacker et al. 2005; Holzer et al. 2008; Helantera et al. 2013) and as a consequence, such colonies will consist of multiple matrilines. However, unlike with the presence of multiple patrilines within a colony, the presence of multiple matrilines will not only generate conflict between nuclear genes, but also between nuclear genes and symbiont genes. In a monogynous colony of a social hymenopteran, all offspring will share the same strain of any MTS that infects their mother. In this case, as noted by Wenseleers (2001), all individuals within such a colony are clonally related from the perspective of an MTS, so there should be no selection on MTSs to manipulate larval caste fate. The same reasoning also holds for secondarily polygynous colonies that readopt related queens. However, we suggest that the presence of multiple maternal lineages introduces the potential for intra-colony conflict between infected and uninfected lineages. Any strain that causes its host to preferentially produce queens will be at a selective advantage compared to queens that are uninfected or infected by a strain that does not bias caste determination; they will not have to pay the cost of producing workers, but will still be able to produce queens, and so will have a greater reproductive output.

This situation is not without precedent. At its simplest, a subset of queens in certain species appear to selfishly contribute more to the production of sexual offspring, and less to the production of new workers (Ross 1988; Fournier et al. 2004). In addition, alternative reproductive morphs, including varying degrees of queen dimorphism, are surprisingly common in ants (Heinze and Tsuji 1995; Heinze and Keller 2000). Whilst this might occur for a number of reasons, in at least some cases smaller morphs called microgynes behave as intraspecific social parasites of colonies also inhabited by larger queens called macrogynes (Wolf and Seppä 2016). For instance, in the ant Myrmica rubra, microgynes produce a much higher proportion of queens relative to macrogynes, essentially parasitizing the production of workers by macrogynes (Elmes 1976; Pearson and Child 1980; Leppänen 2012; Schär and Nash 2014). Furthermore, whilst some gene flow still occurs between the microgyne and macrogyne lineages, there is evidence of genetic divergence between the two (Leppänen et al. 2015, 2016). The social parasite Mycocepurus castrator has taken this a step further; it appears to have originated as an intraspecific social parasite of M. goeldii, but has subsequently become entirely reproductively isolated from its host, and the two are now considered to be distinct species (Rabeling et al. 2014).

It may even be the case that MTSs assist in the sympatric speciation of hosts and their social parasites, as well as being a causal factor in the initial selfish production of queens instead of workers. For instance, Wolbachia-induced mating incompatibilities contribute to reproductive isolation between Drosophila recens and its sister species D. subquinaria, acting in concert with behavioral isolation (Shoemaker et al. 1999; Jaenike et al. 2006). In M. rubra, the presence of a parasite queen generally prevents the production of males by host queens, but hosts do still produce males occasionally, and whilst these males appear less inclined to mate with parasite females, they occasionally do so (Leppänen et al. 2016). Infection with an MTS that also induces mating incompatibilities might explain how social parasites can genetically diverge from their hosts in sympatry, as appears to be the case in M. rubra, even when behavioral isolation is incomplete. MTSs could thus not only drive the initial evolution of selfish reproductive behavior, but also assist in the progression from intraspecific parasite to interspecific parasite. We suggest that alternative reproductive morphs, intraspecific social parasites, inquilines and their hosts should be screened for the presence of reproductive parasites to examine this possibility. Subsequent experiments combining antibiotic treatments, quantification of caste ratios and controlled mating between hosts and parasites could reveal whether social insect lineages are infected with caste-biasing MTSs.

Caste-biasing as a means of distorting host sex ratios

A number of sex-ratio-distorting MTSs are found across arthropods (Duron et al. 2008; Engelstädter and Hurst 2009a; Hurst and Frost 2015). Some cause the death of host males at an early embryonic stage, some feminize genetic males, and others induce parthenogenesis in their hosts, all of which lead to female-biased host sex ratios (Werren et al. 2008). These phenotypes have evolved because males are a reproductive dead-end from the perspective of maternally transmitted symbionts, so it is not surprising that they all involve reducing the number of males produced in order to increase the production of females. However, sex ratios in social hymenopterans, in which diploid eggs can develop into workers or queens, is determined as much by the proportion of diploid eggs that develop into queens rather than workers (i.e., the caste ratio) as it is by the relative proportion of haploid and diploid eggs. As discussed earlier, there is mounting evidence that such caste ratios can have a genotypic component (Anderson et al. 2008; Hughes and Boomsma 2008; Schwander et al. 2010).

In some species, genotypic effects on caste determination, and thus caste ratios, can go on to affect colony sex ratios in social insects. In the ant Cardiocondyla kagutsuchi, different genetic lines produce markedly different sex ratios; interestingly, this is due to differences between genetic lines in the likelihood of female larvae developing into reproductives rather than differences in the primary sex ratio between genetic lines (Frohschammer and Heinze 2009). MTSs in social hymenopterans could employ a very similar strategy, distorting host sex ratios by altering the caste fate of developing larvae such that female larvae are more likely to develop into queens than workers. Evidence for such an effect has recently been found in the ant Monomorium pharaonis. Experimental crosses between Wolbachia-infected and uninfected lineages have shown that infected colonies have more female-biased sex ratios than uninfected colonies and, whilst this is largely driven by reduced production of males in infected colonies, there also appeared to be a weaker effect of infection on caste ratio, with infected colonies producing more reproductive females relative to workers (Pontieri et al. 2016). Future tests of caste-biasing by MTSs as a means of distorting host sex ratios will require further comparisons of caste and sex ratios either in natural populations of mixed infection status, or in experimental populations in which infection status has been manipulated to allow caste and sex ratios to be compared whilst controlling for both host genetic background and environmental effects.

Symbiont-induced thelytokous parthenogenesis and caste determination in the social hymenoptera

In some ant species, caste is determined entirely by the mode of reproduction; workers are produced via sexual reproduction, whilst queens are produced by thelytokous parthenogenesis (Fournier et al. 2005; Leniaud et al. 2012). At least three different MTSs are capable of inducing thelytokous parthenogenesis in arthropods (Ma and Schwander 2017), and so MTSs could, in theory, control caste determination by altering the mode of host reproduction. However, a number of obligately and facultatively parthenogenetic social hymenopterans have been screened for Wolbachia and other symbionts known to induce thelytokous parthenogenesis, and none appear to be infected (Grasso et al. 2000; Wenseleers and Billen 2000; Himler et al. 2009; Kronauer et al. 2012; Martinez-Rodriguez et al. 2013; Rabeling and Kronauer 2013). Initially, symbiont-induced parthenogenesis was thought to proceed only via gamete duplication, which eliminates genomic heterozygosity entirely (Ma and Schwander 2017). Because the majority of social hymenopterans utilize single-locus complimentary sex determination, gamete duplication would lead to the production of sterile diploid males instead of females, and so parthenogenesis-inducing symbionts were assumed to be unable to invade social hymenopterans (van Wilgenburg et al. 2006). However, it is now understood that a variety of cellular mechanisms underlie symbiont-induced parthenogenesis, some of which preserve heterozygosity (Ma and Schwander 2017) and so it is our opinion that the predominance of single-locus complimentary sex determination is not a sufficient explanation for the absence of symbiont-induced parthenogenesis in the social hymenoptera.

Alternatively, it has been proposed that symbiont-induced parthenogenesis is rare in the social hymenoptera for two related reasons, dependent on whether or not workers are sterile (Goudie and Oldroyd 2018). In species with sterile workers, thelytokous reproduction by queens would result in a loss of genetic variation in the worker caste, leaving the species more prone to extinction due to factors such as the accumulation of deleterious mutations and a reduced ability to adapt to fluctuating biotic and abiotic environmental factors (Maynard Smith 1978; Normark et al. 2003; Ross et al. 2013), as well as by removing the more specific benefits provided by a genetically variable worker caste, such as enhanced disease resistance and worker task specialization, rendering the species less competitive in relation to lineages that reproduce sexually (Wiernasz et al. 2008; Goudie and Oldroyd 2018). In species with workers that are not sterile, symbionts will likely cause parthenogenesis in workers as well as queens, precipitating a collapse in reproductive division of labor (Goudie and Oldroyd 2018). More generally, for thelytokous parthenogenesis to play a role in caste determination, it must be facultative, and with the exception of Trichogramma wasps, facultative sex has not been observed in species infected with parthenogenesis-inducing symbionts (Ma and Schwander 2017). In conclusion, MTSs are highly unlikely to affect caste determination in the social hymenoptera by inducing parthenogenesis in their hosts.

Is caste-biasing likely to evolve in practice?

It could be argued that MTSs have only evolved a limited number of manipulative phenotypes, i.e., cytoplasmic incompatibility, male-killing, feminization and parthenogenesis induction, during the course of tens of millions of years of evolutionary history in association with an enormous number of arthropod hosts (Engelstädter and Hurst 2009a; Gerth et al. 2014); perhaps then, it is unparsimonious to propose another origin of a manipulative phenotype. However, it is important to note that the different manipulative phenotypes are, in reality, broad categories describing outcomes in the host, and the cellular and molecular mechanisms underlying reproductive manipulations vary enormously across hosts and MTS strains (Hurst and Frost 2015). For instance, symbiont-induced parthenogenesis proceeds through at least four different cellular mechanisms in arthropods (Ma and Schwander 2017) suggesting independent origins of the phenotype. Furthermore, even when the cellular mechanisms of a manipulative phenotype are the same, the underlying molecular mechanisms may vary, again due to independent origins of the manipulative phenotype (Ma et al. 2014). For example, symbiont-induced cytoplasmic incompatibility is known to occur in at least three distinct bacterial taxa (Engelstädter and Hurst 2009a; Takano et al. 2017). The cytological mechanisms of these mating incompatibilities have been studied in hosts infected with Wolbachia and Cardinium, and are remarkably similar regardless of which symbiont the host is infected with (Gebiola et al. 2017), but comparisons of the genomes of incompatibility-inducing Wolbachia and Cardinium provide no evidence for shared genes underlying the induction of mating incompatibilities; cytoplasmic incompatibility thus appears to have (at the very least) two independent evolutionary origins, rather than a single origin followed by horizontal gene transfer between taxa (Penz et al. 2012). We argue that the limited number of categories of manipulative phenotypes are thus likely to represent many independent origins of manipulative phenotypes, and should not be taken to suggest that MTSs have limited evolutionary potential. In fact, quite the opposite appears to be the case; when the selective conditions are appropriate, MTSs appear readily able to evolve the ability to manipulate host biology through a range of different cellular and molecular mechanisms.

Conclusions

Caste determination in social hymenopterans is increasingly recognized as a complex phenomenon, with multiple interacting causes. We suggest that heritable symbionts should also be considered as additional factors that may influence caste determination, because there are at least three distinct evolutionary scenarios that could select for caste-biasing genes in MTSs. Such symbionts are extremely widespread, easy to detect using a range of standard laboratory techniques, and all three evolutionary scenarios outlined here generate testable predictions concerning caste determination in social hymenopterans. Maternally transmitted symbionts are already renowned for their ability to influence fundamental aspects of metabolism, immunity, behavior and reproduction in their hosts and we suspect that caste determination will be no exception to this.

Notes

Acknowledgements

We would like to thank Joanne Carnell and Rosaline Hulse for comments. This work was funded by the University of Sussex and by a Marie Curie fellowship to TP.

References

  1. Anderson KE, Linksvayer TA, Smith CR (2008) The causes and consequences of genetic caste determination in ants (Hymenoptera: Formicidae). Myrmecol News 11:119–132Google Scholar
  2. Beeman RW, Friesen KS, Denell RE (1992) Maternal effect selfish genes in flour beetles. Science 256:89–92CrossRefPubMedGoogle Scholar
  3. Bennett GM, Moran NA (2015) Heritable symbiosis: the advantages and perils of an evolutionary rabbit hole. Proc Natl Acad Sci 112(33):10169–10176CrossRefPubMedGoogle Scholar
  4. Bourke AF, Ratnieks FL (1999) Kin conflict over caste determination in social Hymenoptera. Behav Ecol Sociobiol 46:287–297CrossRefGoogle Scholar
  5. Brown W, Liautard C, Keller L (2003) Sex-ratio dependent execution of queens in polygynous colonies of the ant Formica exsecta. Oecologia 134:12–17CrossRefPubMedGoogle Scholar
  6. Carew ME, Tay WT, Crozier RH (1997) Polygyny via unrelated queens indicated by mitochondrial DNA variation in the Australian meat ant Iridomyrmex purpureus. Insectes Soc 44:7–14CrossRefGoogle Scholar
  7. Cordaux R, Bouchon D, Grève P (2011) The impact of endosymbionts on the evolution of host sex-determination mechanisms. Trends Genet 27:332–341CrossRefPubMedGoogle Scholar
  8. Crespi BJ, Yanega D (1995) The definition of eusociality. Behav Ecol 6:109–115CrossRefGoogle Scholar
  9. Darras H, Kuhn A, Aron S (2014) Genetic determination of female castes in a hybridogenetic desert ant. J Evol Biol 27:2265–2271CrossRefPubMedGoogle Scholar
  10. de Oliveira CD, Gonçalves DS, Baton LA et al (2015) Broader prevalence of Wolbachia in insects including potential human disease vectors. Bull Entomol Res 105:305–315CrossRefPubMedGoogle Scholar
  11. Duron O, Hurst GDD (2013) Arthropods and inherited bacteria: from counting the symbionts to understanding how symbionts count. BMC Biol 11:45CrossRefPubMedPubMedCentralGoogle Scholar
  12. Duron O, Bouchon D, Boutin S et al (2008) The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol 6:27CrossRefPubMedPubMedCentralGoogle Scholar
  13. Dykstra HR, Weldon SR, Martinez AJ et al (2014) Factors limiting the spread of the protective symbiont Hamiltonella defensa in Aphis craccivora aphids. Appl Environ Microbiol 80:5818–5827CrossRefPubMedPubMedCentralGoogle Scholar
  14. Elmes GW (1976) Some observations on the microgyne form of Myrmica rubra. Insectes Soc 23:3–22CrossRefGoogle Scholar
  15. Engelstädter J, Hurst GDD (2009a) The ecology and evolution of microbes that manipulate host reproduction. Annu Rev Ecol Evol Syst 40:127–149CrossRefGoogle Scholar
  16. Engelstädter J, Hurst GDD (2009b) What use are male hosts? The dynamics of maternally inherited bacteria showing sexual transmission or male killing. Am Nat 173:159–170CrossRefGoogle Scholar
  17. Evans JD (1996) Competition and relatedness between queens of the facultatively polygynous ant Myrmica tahoensis. Anim Behav 51:831–840CrossRefGoogle Scholar
  18. Evison SE, Roberts KE, Laurenson L et al (2012) Pervasiveness of parasites in pollinators. PloS One 7:e30641CrossRefPubMedPubMedCentralGoogle Scholar
  19. Fournier D, Aron S, Keller L (2004) Significant reproductive skew in the facultatively polygynous ant Pheidole pallidula. Mol Ecol 13:203–210CrossRefPubMedGoogle Scholar
  20. Fournier D, Estoup A, Orivel J et al (2005) Clonal reproduction by males and females in the little fire ant. Nature 435:1230–1234CrossRefPubMedGoogle Scholar
  21. Frohschammer S, Heinze J (2009) A heritable component in sex ratio and caste determination in a Cardiocondyla ant. Front Zool 6:27CrossRefPubMedPubMedCentralGoogle Scholar
  22. Frost CL, Fernández-Marín H, Smith JE, Hughes WOH (2010) Multiple gains and losses of Wolbachia symbionts across a tribe of fungus-growing ants. Mol Ecol 19:4077–4085CrossRefPubMedGoogle Scholar
  23. Gebiola M, Giorgini M, Kelly SE et al (2017) Cytological analysis of cytoplasmic incompatibility induced by Cardinium suggests convergent evolution with its distant cousin Wolbachia. Proc R Soc B Biol Sci 284:20171433CrossRefGoogle Scholar
  24. Gerth M, Gansauge M-T, Weigert A, Bleidorn C (2014) Phylogenomic analyses uncover origin and spread of the Wolbachia pandemic. Nat Commun 5:5117CrossRefPubMedGoogle Scholar
  25. Gerth M, Röthe J, Bleidorn C (2013) Tracing horizontal Wolbachia movements among bees (Anthophila): a combined approach using multilocus sequence typing data and host phylogeny. Mol Ecol 22:6149–6162CrossRefPubMedGoogle Scholar
  26. Gerth M, Saeed A, White JA, Bleidorn C (2015) Extensive screen for bacterial endosymbionts reveals taxon-specific distribution patterns among bees (Hymenoptera, Anthophila). FEMS Microbiol Ecol 91:fiv047CrossRefPubMedGoogle Scholar
  27. Goudie F, Oldroyd BP (2018) The distribution of thelytoky, arrhenotoky and androgenesis among castes in the eusocial Hymenoptera. Insectes Soc 65:5–16CrossRefGoogle Scholar
  28. Graham RI, Wilson K (2012) Male-killing Wolbachia and mitochondrial selective sweep in a migratory African insect. BMC Evol Biol 12:204CrossRefPubMedPubMedCentralGoogle Scholar
  29. Grasso DA, Wenseleers T, Mori A et al (2000) Thelytokous worker reproduction and lack of Wolbachia infection in the harvesting ant Messor capitatus. Ethol Ecol Evol 12:309–314CrossRefGoogle Scholar
  30. Hacker M, Kaib M, Bagine RKN et al (2005) Unrelated queens coexist in colonies of the termite Macrotermes michaelseni. Mol Ecol 14:1527–1532CrossRefPubMedGoogle Scholar
  31. Heinze J, Keller L (2000) Alternative reproductive strategies: a queen perspective in ants. Trends Ecol Evol 15:508–512CrossRefPubMedGoogle Scholar
  32. Heinze J, Tsuji K (1995) Ant reproductive strategies. Res Popul Ecol 37:135–149CrossRefGoogle Scholar
  33. Helantera H, Aehle O, Roux M et al (2013) Family-based guilds in the ant Pachycondyla inversa. Biol Lett 9:20130125CrossRefPubMedPubMedCentralGoogle Scholar
  34. Himler AG, Caldera EJ, Baer BC et al (2009) No sex in fungus-farming ants or their crops. Proc R Soc B Biol Sci 276:2611–2616CrossRefGoogle Scholar
  35. Hoffmann AA, Turelli M, Harshman LG (1990) Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics 126:933–948PubMedPubMedCentralGoogle Scholar
  36. Holzer B, Chapuisat M, Keller L (2008) Foreign ant queens are accepted but produce fewer offspring. Oecologia 157:717–723CrossRefPubMedGoogle Scholar
  37. Hughes WOH, Boomsma JJ (2007) Genetic polymorphism in leaf-cutting ants is phenotypically plastic. Proc R Soc B Biol Sci 274:1625–1630CrossRefGoogle Scholar
  38. Hughes WOH, Boomsma JJ (2008) Genetic royal cheats in leaf-cutting ant societies. Proc Natl Acad Sci 105:5150–5153CrossRefPubMedPubMedCentralGoogle Scholar
  39. Hurst GDD, Frost CL (2015) Reproductive parasitism: maternally inherited symbionts in a biparental world. Cold Spring Harb Perspect Biol 7:a017699CrossRefPubMedPubMedCentralGoogle Scholar
  40. Hurst GDD, Jiggins FM, Robinson SJW (2001) What causes inefficient transmission of male-killing Wolbachia in Drosophila? Heredity 87:220–226CrossRefPubMedGoogle Scholar
  41. Jaenike J, Dyer KA, Cornish C, Minhas MS (2006) Asymmetrical reinforcement and Wolbachia infection in Drosophila. PLoS Biol 4:e325CrossRefPubMedPubMedCentralGoogle Scholar
  42. Julian GE, Fewell JH, Gadau J et al (2002) Genetic determination of the queen caste in an ant hybrid zone. Proc Natl Acad Sci 99:8157–8160CrossRefPubMedGoogle Scholar
  43. Kautz S, Rubin BER, Moreau CS (2013) Bacterial infections across the ants: frequency and prevalence of Wolbachia, Spiroplasma, and Asaia. Psyche (Stuttg) 2013:1–11CrossRefGoogle Scholar
  44. Keller L, Liautard C, Reuter M et al (2001) Sex ratio and Wolbachia infection in the ant Formica exsecta. Heredity 87:227–233CrossRefPubMedGoogle Scholar
  45. Kronauer DJC, Pierce NE, Keller L (2012) Asexual reproduction in introduced and native populations of the ant Cerapachys biroi. Mol Ecol 21:5221–5235CrossRefPubMedGoogle Scholar
  46. Kuhn A, Darras H, Aron S (2018) Phenotypic plasticity in an ant with strong caste–genotype association. Biol Lett 14:20170705CrossRefPubMedGoogle Scholar
  47. Leniaud L, Darras H, Boulay R, Aron S (2012) Social hybridogenesis in the clonal ant Cataglyphis hispanica. Curr Biol 22:1188–1193CrossRefPubMedGoogle Scholar
  48. Leppänen J (2012) Genetic differentiation between the ant Myrmica rubra and its microgynous social parasite. University of HelsinkiGoogle Scholar
  49. Leppänen J, Seppä P, Vepsäläinen K, Savolainen R (2016) Mating isolation between the ant Myrmica rubra and its microgynous social parasite. Insectes Soc 63:79–86CrossRefGoogle Scholar
  50. Leppänen J, Seppä P, Vepsäläinen K, Savolainen R (2015) Genetic divergence between the sympatric queen morphs of the ant Myrmica rubra. Mol Ecol 24:2463–2476CrossRefPubMedGoogle Scholar
  51. Ma W-J, Schwander T (2017) Patterns and mechanisms in instances of endosymbiont-induced parthenogenesis. J Evol Biol 30:868–888CrossRefPubMedGoogle Scholar
  52. Ma W-J, Vavre F, Beukeboom LW (2014) Manipulation of arthropod sex determination by endosymbionts: diversity and molecular mechanisms. Sex Dev 8:59–73CrossRefPubMedGoogle Scholar
  53. Martinez-Rodriguez P, Sarasa J, Peco B et al (2013) Endosymbiont-free ants: molecular biological evidence that neither Wolbachia, Cardinium or any other bacterial endosymbionts play a role in thelytokous parthenogenesis in the harvester ant species, Messor barbarus and M. capitatus (Hymenoptera: Formicidae). Eur J Entomol 110:197–204CrossRefGoogle Scholar
  54. Maynard Smith J (1978) The evolution of sex. Cambridge University Press, CambridgeGoogle Scholar
  55. Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190CrossRefPubMedGoogle Scholar
  56. Moritz RFA, Lattorff HMG, Neumann P et al (2005) Rare royal families in honeybees, Apis mellifera. Naturwissenschaften 92:488–491CrossRefPubMedGoogle Scholar
  57. Normark BB, Judson OP, Moran NA (2003) Genomic signatures of ancient asexual lineages. Biol J Linn Soc 79:69–84CrossRefGoogle Scholar
  58. Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci 100:1803–1807CrossRefPubMedGoogle Scholar
  59. Oliver KM, Smith AH, Russell JA (2014) Defensive symbiosis in the real world—advancing ecological studies of heritable, protective bacteria in aphids and beyond. Funct Ecol 28:341–355CrossRefGoogle Scholar
  60. Oster GF, Wilson EO (1979) Caste and ecology in the social insects. Princeton University Press, PrincetonGoogle Scholar
  61. Pearson B, Child AR (1980) The distribution of an esterase polymorphism in macrogynes and microgynes of Myrmica rubra Latreille. Evolution 34:105CrossRefPubMedGoogle Scholar
  62. Penz T, Schmitz-Esser S, Kelly SE et al (2012) Comparative genomics suggests an independent origin of cytoplasmic incompatibility in Cardinium hertigii. PLoS Genet 8:e1003012CrossRefPubMedPubMedCentralGoogle Scholar
  63. Pontieri L, Schmidt AM, Singh R et al (2016) Artificial selection on ant female caste ratio uncovers a link between female-biased sex ratios and infection by Wolbachia endosymbionts. J Evol Biol 30:225–234CrossRefPubMedGoogle Scholar
  64. Rabeling C, Kronauer DJC (2013) Thelytokous parthenogenesis in eusocial hymenoptera. Annu Rev Entomol 58:273–292CrossRefPubMedGoogle Scholar
  65. Rabeling C, Schultz TR, Pierce NE, Bacci M (2014) A social parasite evolved reproductive isolation from its fungus-growing ant host in sympatry. Curr Biol 24:2047–2052CrossRefPubMedGoogle Scholar
  66. Ratnieks FL, Foster KR, Wenseleers T (2006) Conflict resolution in insect societies. Annu Rev Entomol 51:581–608CrossRefPubMedGoogle Scholar
  67. Ross KG (1988) Differential reproduction in multiple-queen colonies of the fire ant Solenopsis invicta (Hymenoptera: Formicidae). Behav Ecol Sociobiol 23:341–355CrossRefGoogle Scholar
  68. Ross L, Hardy NB, Okusu A, Normark BB (2013) Large population size predicts the distribution of asexuality in scale insects. Evolution 67:196–206CrossRefPubMedGoogle Scholar
  69. Roy V, Girondot M, Harry M (2015) The distribution of Wolbachia in Cubitermes (Termitidae, Termitinae) castes and colonies: a modelling approach. PLoS ONE 10:e0116070CrossRefPubMedPubMedCentralGoogle Scholar
  70. Russell JA (2012) The ants (Hymenoptera: Formicidae) are unique and enigmatic hosts of Wolbachia (Alphaproteobacteria) symbionts. Myrmecol News 16:7–23Google Scholar
  71. Russell JA, Funaro CF, Giraldo YM et al (2012) A veritable menagerie of heritable bacteria from ants, butterflies, and beyond: broad molecular surveys and a systematic review. PLoS One 7:e51027CrossRefPubMedPubMedCentralGoogle Scholar
  72. Russell JA, Goldman-Huertas B, Moreau CS et al (2009) Specialization and geographic isolation among Wolbachia symbionts from ants and lycaenid butterflies. Evolution 63:624–640CrossRefPubMedGoogle Scholar
  73. Scarborough CL, Ferrari J, Godfray HCJ (2005) Aphid protected from pathogen by endosymbiont. Science 310:1781–1781CrossRefPubMedGoogle Scholar
  74. Schär S, Nash DR (2014) Evidence that microgynes of Myrmica rubra ants are social parasites that attack old host colonies. J Evol Biol 27:2396–2407CrossRefPubMedGoogle Scholar
  75. Schwander T, Keller L (2008) Genetic compatibility affects queen and worker caste determination. Science 322:552–552CrossRefPubMedGoogle Scholar
  76. Schwander T, Lo N, Beekman M et al (2010) Nature versus nurture in social insect caste differentiation. Trends Ecol Evol 25:275–282CrossRefPubMedGoogle Scholar
  77. Shigenobu S, Watanabe H, Hattori M et al (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS Nature 407:81–86CrossRefPubMedGoogle Scholar
  78. Shoemaker DD, Ahrens M, Sheill L et al (2003) Distribution and prevalence of Wolbachia infections in native populations of the fire ant Solenopsis invicta (Hymenoptera: Formicidae). Environ Entomol 32:1329–1336CrossRefGoogle Scholar
  79. Shoemaker DD, Katju V, Jaenike J (1999) Wolbachia and the evolution of reproductive isolation between Drosophila recens and Drosophila subquinaria. Evolution 53:1157–1164CrossRefPubMedGoogle Scholar
  80. Sikulu-Lord MT, Maia MF, Milali MP et al (2016) Rapid and non-destructive detection and identification of two strains of Wolbachia in Aedes aegypti by near-infrared spectroscopy. PLoS Negl Trop Dis 10:e0004759CrossRefPubMedPubMedCentralGoogle Scholar
  81. Stille M, Stille B (1992) Intra- and inter-nest variation in mitochondrial DNA in the polygynous ant Leptothorax acervorum (Hymenoptera: Formicidae). Insectes Soc 39:335–340CrossRefGoogle Scholar
  82. Takano S, Tuda M, Takasu K et al (2017) Unique clade of alphaproteobacterial endosymbionts induces complete cytoplasmic incompatibility in the coconut beetle. Proc Natl Acad Sci 114:6110–6115CrossRefPubMedPubMedCentralGoogle Scholar
  83. Van Borm S, Wenseleers T, Billen J, Boomsma JJ (2001) Wolbachia in leafcutter ants: a widespread symbiont that may induce male killing or incompatible matings. J Evol Biol 14:805–814CrossRefGoogle Scholar
  84. van Wilgenburg E, Driessen G, Beukeboom LW (2006) Single locus complementary sex determination in Hymenoptera: an “unintelligent” design? Front Zool 3:1CrossRefPubMedPubMedCentralGoogle Scholar
  85. Weinert LA, Araujo-Jnr EV, Ahmed MZ, Welch JJ (2015) The incidence of bacterial endosymbionts in terrestrial arthropods. Proc R Soc B Biol Sci 282:20150249CrossRefGoogle Scholar
  86. Wenseleers T (2001) Conflict from cell to colony. Katholieke Universitiet LeuvenGoogle Scholar
  87. Wenseleers T, Billen J (2000) No evidence for Wolbachia-induced parthenogenesis in the social Hymenoptera. J Evol Biol 13:277–280CrossRefGoogle Scholar
  88. Wenseleers T, Ito F, Van Borm S et al (1998) Widespread occurrence of the microorganism Wolbachia in ants. Proc R Soc B Biol Sci 265:1447–1452CrossRefGoogle Scholar
  89. Wenseleers T, Sundstrom L, Billen J (2002) Deleterious Wolbachia in the ant Formica truncorum. Proc R Soc B Biol Sci 269:623–629CrossRefGoogle Scholar
  90. Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751CrossRefPubMedGoogle Scholar
  91. Werren JH, O’Neill SL (1997) The evolution of heritable symbionts. In: influential passengers: inherited microorganisms and arthropod reproduction. Oxford University Press, Oxford, pp 1–41Google Scholar
  92. Wiernasz DC, Hines J, Parker DG, Cole BJ (2008) Mating for variety increases foraging activity in the harvester ant, Pogonomyrmex occidentalis. Mol Ecol 17:1137–1144CrossRefPubMedGoogle Scholar
  93. Wilson EO (1971) The insect societies. Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  94. Wolf JI, Seppä P (2016) Queen size dimorphism in social insects. Insectes Soc 63:25–38CrossRefGoogle Scholar

Copyright information

© The Author(s) 2018

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  1. 1.School of Life SciencesUniversity of SussexBrightonUK

Personalised recommendations