Biodiversity, host specificity, and dominance by eusocial species among sponge-dwelling alpheid shrimp on the Belize Barrier Reef

Alpheid shrimp represent an abundant and diverse, but poorly characterized, component of the cryptic biodiversity of coral reefs worldwide. Sponge‐inhabiting alpheids provide a promising model system for exploring patterns of cryptic reef biodiversity because their habitats (hosts) are discrete and qualitatively distinct units. We tabulated data from 14 years of collections at Carrie Bow Cay, Belize to quantify patterns of diversity, host specificity, and dominance among sponge‐dwelling shrimp (Synalpheus), with special attention to eusocial species. From > 600 sampled sponges of 17 species, we recognized at least 36 Synalpheus shrimp species. Of these, 15 (42%) were new to science. Species accumulation curves suggest that we have sampled most of the Synalpheus diversity at Carrie Bow Cay. Diversity of sponge‐dwelling Synalpheus was slightly higher in shallow water, probably because of greater habitat diversity, than in deep water. Host specificity was surprisingly high, with > 50% of all shrimp species found in only a single sponge species each, although some shrimp species used as many as six hosts. Cohabitation of individual sponges by multiple shrimp species was rarer than expected by chance, supporting previous distributional and behavioural evidence that competition for hosts is strong and moulds patterns of host association. The fauna of most well‐sampled sponge species was dominated, both in numbers of individuals and in frequency of occurrence, by eusocial species. Eusocial shrimp species also inhabited a significantly greater number of sponge species than did non‐social shrimp. Consequently, > 65% of shrimp in our quantitative samples belonged to the four eusocial species, and on a per‐species basis, eusocial species were 17 times as abundant as non‐social species. Our data suggest that the highly diverse sponge‐dwelling shrimp assemblage of the Belize Barrier Reef is structured by competition, and that eusociality has allowed a small number of species to dominate the sponge resource.     

Eusociality Shapes Convergent Patterns of Molecular Evolution across Mitochondrial Genomes of Snapping Shrimps

Eusociality is a highly conspicuous and ecologically impactful behavioral syndrome that has evolved independently across multiple animal lineages. So far, comparative genomic analyses of advanced sociality have been mostly limited to insects. Here, we study the only clade of animals known to exhibit eusociality in the marine realm—lineages of socially diverse snapping shrimps in the genus Synalpheus. To investigate the molecular impact of sociality, we assembled the mitochondrial genomes of eight Synalpheus species that represent three independent origins of eusociality and analyzed patterns of molecular evolution in protein-coding genes. Synonymous substitution rates are lower and potential signals of relaxed purifying selection are higher in eusocial relative to noneusocial taxa. Our results suggest that mitochondrial genome evolution was shaped by eusociality-linked traits—extended generation times and reduced effective population sizes that are hallmarks of advanced animal societies. This is the first direct evidence of eusociality impacting genome evolution in marine taxa. Our results also strongly support the idea that eusociality can shape genome evolution through profound changes in life history and demography.     

Multiple origins of eusociality among sponge-dwelling shrimps (Synalpheus)

Abstract.— As the most extreme expression of apparent altruism in nature, eusociality has long posed a central paradox for behavioral and evolutionary ecology. Because eusociality has arisen rarely among animals, understanding the selective pressures important in early stages of its evolution remains elusive. Employing a historical approach to this problem, we used morphology and DNA sequences to reconstruct the phylogeny of 13 species of sponge-dwelling shrimps ( Synalpheus ) with colony organization ranging from asocial pair-bonding through eusociality. We then used phylogenetically independent contrasts to test whether sociality was associated with evidence of enhanced competitive ability, as suggested by hypotheses invoking an advantage of cooperation in crowded habitats. The molecular, morphological, and combined data each strongly supported three independent origins of monogynous, multigenerational (eusocial) colony organization within this genus. Phylogenetically independent contrasts confirmed that highly social taxa, with strong reproductive skew, have significantly higher relative abundance within the host sponge than do less social taxa, a result that was robust to uncertainty in tree topology and varying models of character change. A similar tendency for highly social species to share their sponge with fewer congener species was suggestive, but not significant. Because unoccupied habitat appears to be limiting for many sponge-dwelling shrimp species, these data are consistent with hypotheses that cooperative social groups enjoy a competitive advantage over less organized groups or individuals, where independent establishment is difficult, and that enemy pressure is of central importance in the evolution of animal sociality.     

Subsociality in halictine bees

To look for the occurrence and the significance of brood care in social evolution, I reared six eusocial halictine bee species in laboratory cages enabling the observation of intranest behaviour: Lasioglossum (Evylaeus) laticeps, L. (E.) pauxillum, L. (E.) nigripes, L. (E.) euboeensis, Halictus (Halictus) scabiosae and L. (E.) fulvicorne. All of them were subsocial, each mother caring for her brood. Brood cells were sealed after oviposition with earthen plugs; they were then reopened, visited and closed again. These observations plus the reports in the literature on eleven eusocial species indicate that seventeen species of eusocial halictine bees provide parental care, i.e. are subsocial. Brood care, subsociality, is strongly associated with eusociality. To study reversal from eusociality to subsociality, I have reared the non-eusocial form of two species within which there are or have been eusocial forms: Halictus (H.) rubicundus and Lasioglossum (E.) fratellum. They are secondarily solitary, having lost worker brood. However, both species still show brood care. This suggests that in transitions to eusociality, brood care antedated eusociality. To further examine this issue I reared two truly solitary species that are not derived from eusocial ancestors: Lasioglossum (E.) villosulum and L. (L.) quadrinotatum. Unlike secondarily solitary species, females of both these species close their brood cells after oviposition and ignore their progeny thereafter. This association strongly suggests that the subsocial route with maternal brood care is the route to eusociality in halictine bees.     

Specialization and generalization in the diversification of phytophagous insects: tests of the musical chairs and oscillation hypotheses

Evolutionary biologists have often assumed that ecological generalism comes at the expense of less intense exploitation of specific resources and that this trade-off will promote the evolution of ecologically specialized daughter species. Using a phylogenetic comparative approach with butterflies as a model system, we test hypotheses that incorporate changes in niche breadth and location into explanations of the taxonomic diversification of insect herbivores. Specifically, we compare the oscillation hypothesis, where speciation is driven by host-plant generalists giving rise to specialist daughter species, to the musical chairs hypothesis, where speciation is driven by host-plant switching, without changes in niche breadth. Contrary to the predictions of the oscillation hypothesis, we recover a negative relationship between host-plant breadth and diversification rate and find that changes in host breadth are seldom coupled to speciation events. By contrast, we present evidence for a positive relationship between rates of host switching and butterfly diversification, consonant with the musical chairs hypothesis. These results suggest that the costs of trophic generalism in plant-feeding insects may have been overvalued and that transitions from generalists to ecological specialists may not be an important driver of speciation in general.     

Reproductive skew drives patterns of sexual dimorphism in sponge-dwelling snapping shrimps

Sexual dimorphism is typically a result of strong sexual selection on male traits used in male–male competition and subsequent female choice. However, in social species where reproduction is monopolized by one or a few individuals in a group, selection on secondary sexual characteristics may be strong in both sexes. Indeed, sexual dimorphism is reduced in many cooperatively breeding vertebrates and eusocial insects with totipotent workers, presumably because of increased selection on female traits. Here, we examined the relationship between sexual dimorphism and sociality in eight species of Synalpheus snapping shrimps that vary in social structure and degree of reproductive skew. In species where reproduction was shared more equitably, most members of both sexes were physiologically capable of breeding. However, in species where reproduction was monopolized by a single individual, a large proportion of females—but not males—were reproductively inactive, suggesting stronger reproductive suppression and conflict among females. Moreover, as skew increased across species, proportional size of the major chela—the primary antagonistic weapon in snapping shrimps—increased among females and sexual dimorphism in major chela size declined. Thus, as reproductive skew increases among Synalpheus, female–female competition over reproduction appears to increase, resulting in decreased sexual dimorphism in weapon size.     

Ecological constraints drive social evolution in the African mole-rats.

The African mole-rats (family Bathyergidae) are subterranean hystricomorph rodents occurring in a variety of habitats and displaying levels of sociality which range from solitary to eusocial, making them a unique mammalian taxonomic group to test ecological influences on sociality. Here, we use an extensive DNA-based phylogeny and comparative analysis to investigate the relationship between ecology, sociality and evolution within the family. Mitochondrial cytochrome-b and 12s rRNA trees reveal that the solitary species are monophyletic when compared to the social species. The naked mole-rat (Heterocephalus glaber) is ancestral and divergent from the Damaraland mole-rat (Cryptomys damarensis), supporting previous findings that have suggested the multiple evolution of eusociality within the family. The Cryptomys genus is species-rich and contains taxa exhibiting different levels of sociality, which can be divided into two distinct clades. A total of seven independent comparisons were generated within the phylogeny, and three ecological variables were significantly correlated with social group size: geophyte density (p < 0.05), mean months per year of rainfall greater than 25 mm (p < 0.001), and the coefficient of rainfall variation (p = 0.001). These results support the food-aridity hypothesis for the evolution of highly social cooperative behaviour in the Bathyergidae, and are consistent with the current theoretical framework for skew theory.     

Decline and Local Extinction of Caribbean Eusocial Shrimp

The tropical shrimp genus Synalpheus includes the only eusocial marine animals. In much of the Caribbean, eusocial species have dominated the diverse fauna of sponge-dwelling shrimp in coral rubble for at least the past two decades. Here we document a recent, dramatic decline and apparent local extinction of eusocial shrimp species on the Belize Barrier Reef. Our collections from shallow reefs in central Belize in 2012 failed to locate three of the four eusocial species formerly abundant in the area, and showed steep declines in colony size and increases in frequency of queenless colonies prior to their disappearance. Concordant with these declines, several nonsocial, pair-forming Synalpheus species increased in frequency. The decline in eusocial shrimp is explained in part by disappearance of two sponge species on which they specialize. Eusocial shrimp collections from Jamaica in 2012 showed similar patterns of decline in colony size and increased queenlessness compared with prior Jamaican collections. The decline and local extinction of eusocial shrimp happened against a backdrop of changes in coral assemblages during recent decades, and may reflect changes in abundance and quality of dead coral substratum and succession of the diverse cryptic organisms living within it. These changes document potentially worrisome declines in a unique taxon of eusocial marine animals.     

Evolutionary association between subterranean lifestyle and female sociality in rodents

Subterranean rodents are a good model system to examine adaptive evolution of social organization. Life underground has been proposed either to favor solitariness or, to the contrary, to promote sociality. In concordance with the first idea, most specialized diggers are solitary. However, group-living in several unrelated subterranean rodent species and especially eusociality in two genera of African mole-rats, the Bathyergidae, seem to support the second hypothesis. Thus, none of the two models is fully consistent with empirical data. Here we apply the comparative phylogenetic method to test an evolutionary correlation between fossoriality and female social strategy (solitary breeding vs breeding in group). Both characters show very strong phylogenetic signal, and we found a significant correlation between them. Subterranean lifestyle is readily acquired under female sociality. By contrast, the transition to life underground is extremely unlikely under female solitariness. Thus, not only social behavior may be affected by ecological specialization as it is widely assumed, but it can itself restrain the range of possible specializations. The rates of transition from sociality to solitariness are equal under subterranean and surface-dwelling lifestyle. Sociality loss is irreversible in subterranean lineages, unlike surface-dwelling lineages. Based on the revealed transition rates we suggest that all lineages of subterranean rodents have gone through the stage of cooperation at the beginning of their evolutionary track, whereas group-living is selected against in highly specialized diggers. An odd pattern of distribution of sociality across and within truly subterranean taxa probably derives from the influence of extrinsic factors in combination with phylogenetic inertia.     

Life history of Kladothrips ellobus and Oncothrips rodwayi: insight into the origin and loss of soldiers in gall-inducing thrips

1. The evolution of eusociality in Australian gall‐inducing thrips cannot be understood without comparisons among closely related solitary species. The life history of two solitary, gall‐inducing thrips, Kladothrips ellobus and Oncothrips rodwayi, was investigated, and data for solitary and eusocial species from previous studies were re‐analysed. Kladothrips ellobus is in a clade that is closely related to the eusocial species. Oncothrips rodwayi is in the same clade as the eusocial species and appears to have undergone an evolutionary loss of eusociality. It is the only galling thrips on Acacia in temperate environments. 2. The brood size of K. ellobus is eight to 23 times larger than broods of foundresses in eusocial species whereas the brood size of O. rodwayi is not significantly different from those of foundresses in eusocial species. 3. In K. ellobus, the mean sex ratio was not significantly different from parity but in O. rodwayi the mean sex ratio was 0.13 male. In O. rodwayi, 77% of females were inseminated by their brothers before dispersal, which is consistent with high levels of inbreeding in eusocial species of the same clade. Sex ratios suggest random mating in K. ellobus whereas female‐biased sex ratios in O. rodwayi are consistent with inbreeding and local mate competition. 4. Comparisons among solitary and eusocial species suggest that large brood size is an ancestral trait for eusociality in thrips, and this trait persists in solitary species as an r‐selection strategy. Soldiers may have evolved in arid environments to minimise the risks of dispersal and the costs of latency to reproduction, and to maximise gall defence. 5. Temperate conditions could have facilitated the evolutionary loss of soldiers in O. rodwayi, as there should be a shorter, safer, more predictable window period between dispersal and gall induction, reducing the period of latency to reproduction following dispersal and lowering risks of dispersal. 6. The loss of soldiers in O. rodwayi is not associated with a reversion to the large brood sizes of solitary species in ancestral lineages.     

The evolution of social inbreeding mating systems in spiders: limited male mating dispersal and lack of pre‐copulatory inbreeding avoidance in a subsocial predecessor

Cooperation and group living are extremely rare in spiders and only few species are known to be permanently social. Inbreeding is a key characteristic of social spiders, resulting in high degrees of within‐colony relatedness that may foster kin‐selected benefits of cooperation. Accordingly, philopatry and regular inbreeding are suggested to play a major role in the repeated independent origins of sociality in spiders. We conducted field observations and laboratory experiments to investigate the mating system of the subsocial spider Stegodyphus tentoriicola. The species is suggested to resemble the ‘missing link’ in the transition from subsociality to permanent sociality in Stegodyphus spiders because its social period is prolonged in comparison to other subsocial species. Individuals in our two study populations were spatially clustered around maternal nests, indicating that clusters consist of family groups as found in the subsocial congener Stegodyphus lineatus. Male mating dispersal was limited and we found no obvious pre‐copulatory inbreeding avoidance, suggesting a high likelihood of mating with close kin. Rates of polygamy were low, a pattern ensuring high relatedness within broods. In combination with ecological constraints, such as high costs of dispersal, our findings are consistent with the hypothesis that the extended social period in S. tentoriicola is accompanied with adaptations that facilitate the transition towards permanent sociality. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98 , 851–859.     

Ploidy of the eusocial beetle Austroplatypus incompertus (Schedl) (Coleoptera, Curculionidae) and implications for the evolution of eusociality

In the hymenopterans, haplodiploidy, leading to high-genetic relatedness amongst full sisters has been regarded as critical to kin selection and inclusive fitness hypotheses that explain the evolution of eusociality and altruistic behaviours. Recent evidence for independent origins of eusociality in phylogenetically diverse taxa has led to the controversy regarding the general importance of relatedness to eusociality and its evolution. Here, we developed a highly polymorphic microsatellite marker to test whether the eusocial ambrosia beetle Austroplatypus incompertus (Schedl) is haplodiploid or diplodiploid. We found that both males and females of A. incompertus are diploid, signifying that altruistic behaviour resulting from relatedness asymmetries did not play a role in the evolution of eusocialty in this species. This provides additional evidence against the haplodiploidy hypothesis and implicates alternative hypotheses for the evolution of eusociality.     

Species pool structure determines the level of generalism of island parasitoid faunas

Aim To examine whether island parasitoid faunas are biased towards generalists when compared with the mainland and their species pool, and to evaluate the effects of climate, island characteristics and regional factors on the relative proportions of idiobionts (i.e. generalists) and koinobionts (i.e. specialists) of two parasitic wasp families, Braconidae and Ichneumonidae. Location Seventy‐three archipelagos distributed world‐wide. Methods We used data on the distribution and biology obtained from a digital catalogue and several literature sources. We related level of generalism, measured as the ratio between the number of idiobiont and koinobiont species, to climatic, physiographic and regional factors using generalized linear models. We compared models by means of Akaike weighting, and evaluated the spatial structure of their residuals. We used partial regressions to determine whether the final models account for all latitudinal structure in the level of generalism. Results Islands host comparatively more idiobionts than continental areas. Although there is a latitudinal gradient in the level of generalism of island faunas correlating with both environmental factors and island characteristics, the most important determinant of island community structure is their source pool. This effect is stronger for ichneumonids, where generalism is higher in the Indomalayan region, arguably due to the higher diversity of endophytic hosts in its large rain forests. Main conclusions The level of generalism of island parasitoid faunas is largely constrained by regional factors, namely by the structure of the species pool, which emphasizes the importance of including regional processes in our understanding of the functioning of ecological communities. The fact that generalist species are more predominant in islands with a large cover of rain forests pinpoints the importance of the indirect effects of ecological requirements on community structure, highlighting the complex nature of geographical gradients of diversity.     

Fruit‐breeding drosophilids (Diptera) in the Neotropics: playing the field and specialising in generalism?

1. Species of Drosophilidae are frequently used as model organisms, but their relationships with the environment, particularly in immature stages, remain poorly known. 2. This is the most comprehensive survey to date of fruit‐breeding drosophilids and their hosts in the Neotropics. Drosophilid host‐utilisation patterns were analysed as to geographic origin (native versus exotic) and level of specialisation. 3. The 180 species of plants recorded as drosophilid hosts are distributed across the main Angiosperm lineages and fleshy‐fruited orders; plant families that hosted the greatest number of drosophilid species were Arecaceae, Moraceae, and Myrtaceae. The 100 nominal drosophilid species recorded breeding in fruits belong to just over one‐third of Neotropical genera; most species (91) belong to Drosophila. Drosophilid species with the greatest resource breadth were Drosophila simulans, Drosophila nebulosa, and Zaprionus indianus. 4. Exotic drosophilids breed in more plant species than Neotropical drosophilids and use exotic hosts more frequently, possibly because they are generalists that have survived the trial of introduction and establishment in the Neotropics. Native drosophilids are more variable in resource breadth and sometimes adopt exotic hosts. 5. Amongst the 49 drosophilids with enough records for analysis (> 4), 48 were categorised as generalists. One possible explanation for such overwhelming generalism is the high diversity of Neotropical habitat or hosts. A second, non‐exclusive explanation, suggested by recent studies and empirically supported by the absence of host specialisation found in this study, is that drosophilids could be selective of the dominant yeasts and bacteria in host tissue, and not of the hosts themselves.     

Sociality and the rate of molecular evolution

The molecular clock does not tick at a uniform rate in all taxa but may be influenced by species characteristics. Eusocial species (those with reproductive division of labor) have been predicted to have faster rates of molecular evolution than their nonsocial relatives because of greatly reduced effective population size; if most individuals in a population are nonreproductive and only one or few queens produce all the offspring, then eusocial animals could have much lower effective population sizes than their solitary relatives, which should increase the rate of substitution of "nearly neutral" mutations. An earlier study reported faster rates in eusocial honeybees and vespid wasps but failed to correct for phylogenetic nonindependence or to distinguish between potential causes of rate variation. Because sociality has evolved independently in many different lineages, it is possible to conduct a more wide-ranging study to test the generality of the relationship. We have conducted a comparative analysis of 25 phylogenetically independent pairs of social lineages and their nonsocial relatives, including bees, wasps, ants, termites, shrimps, and mole rats, using a range of available DNA sequences (mitochondrial and nuclear DNA coding for proteins and RNAs, and nontranslated sequences). By including a wide range of social taxa, we were able to test whether there is a general influence of sociality on rates of molecular evolution and to test specific predictions of the hypothesis: (1) that social species have faster rates because they have reduced effective population sizes; (2) that mitochondrial genes would show a greater effect of sociality than nuclear genes; and (3) that rates of molecular evolution should be correlated with the degree of sociality. We find no consistent pattern in rates of molecular evolution between social and nonsocial lineages and no evidence that mitochondrial genes show faster rates in social taxa. However, we show that the most highly eusocial Hymenoptera do have faster rates than their nonsocial relatives. We also find that social parasites (that utilize the workers from related species to produce their own offspring) have faster rates than their social relatives, which is consistent with an effect of lower effective population size on rate of molecular evolution. Our results illustrate the importance of allowing for phylogenetic nonindependence when conducting investigations of determinants of variation in rate of molecular evolution.     

The antiquity and evolutionary history of social behavior in bees

A long-standing controversy in bee social evolution concerns whether highly eusocial behavior has evolved once or twice within the corbiculate Apidae. Corbiculate bees include the highly eusocial honey bees and stingless bees, the primitively eusocial bumble bees, and the predominantly solitary or communal orchid bees. Here we use a model-based approach to reconstruct the evolutionary history of eusociality and date the antiquity of eusocial behavior in apid bees, using a recent molecular phylogeny of the Apidae. We conclude that eusociality evolved once in the common ancestor of the corbiculate Apidae, advanced eusociality evolved independently in the honey and stingless bees, and that eusociality was lost in the orchid bees. Fossil-calibrated divergence time estimates reveal that eusociality first evolved at least 87 Mya (78 to 95 Mya) in the corbiculates, much earlier than in other groups of bees with less complex social behavior. These results provide a robust new evolutionary framework for studies of the organization and genetic basis of social behavior in honey bees and their relatives.     

The risk‐return trade‐off between solitary and eusocial reproduction

Social insect colonies can be seen as a distinct form of biological organisation because they function as superorganisms. Understanding how natural selection acts on the emergence and maintenance of these colonies remains a major question in evolutionary biology and ecology. Here, we explore this by using multi‐type branching processes to calculate the basic reproductive ratios and the extinction probabilities for solitary vs. eusocial reproductive strategies. We find that eusociality, albeit being hugely successful once established, is generally less stable than solitary reproduction unless large demographic advantages of eusociality arise for small colony sizes. We also demonstrate how such demographic constraints can be overcome by the presence of ecological niches that strongly favour eusociality. Our results characterise the risk‐return trade‐offs between solitary and eusocial reproduction, and help to explain why eusociality is taxonomically rare: eusociality is a high‐risk, high‐reward strategy, whereas solitary reproduction is more conservative.     

Challenging the inbreeding hypothesis in a eusocial mammal: population genetics of the naked mole‐rat,Heterocephalus glaber

The role of genetic relatedness in the evolution of eusociality has been the topic of much debate, especially when contrasting eusocial insects with vertebrates displaying reproductive altruism. The naked mole‐rat, Heterocephalus glaber, was the first described eusocial mammal. Although this discovery was based on an ecological constraints model of eusocial evolution, early genetic studies reported high levels of relatedness in naked mole‐rats, providing a compelling argument that low dispersal rates and consanguineous mating (inbreeding as a mating system) are the driving forces for the evolution of this eusocial species. One caveat to accepting this long‐held view is that the original genetic studies were based on limited sampling from the species’ geographic distribution. A growing body of evidence supports a contrary view, with the original samples not representative of the species—rather reflecting a single founder event, establishing a small population south of the Athi River. Our study is the first to address these competing hypotheses by examining patterns of molecular variation in colonies sampled from north and south of the Athi and Tana rivers, which based on our results, serve to isolate genetically distinct populations of naked mole‐rats. Although colonies south of the Athi River share a single mtDNA haplotype and are fixed at most microsatellite loci, populations north of the Athi River are considerably more variable. Our findings support the position that the low variation observed in naked mole‐rat populations south of the Athi River reflects a founder event, rather than a consequence of this species’ unusual mating system.     

Ecological correlates of sociality in <Emphasis Type="Italic">Pemphigus</Emphasis> aphids,with a partial phylogeny of the genus

Background  

Because the systems of social organisation in the various species of Pemphigus aphids span the continuum from asociality through to advanced sociality (typified by the possession of morphologically specialised soldiers), the genus is an ideal model clade in which to study the influence of ecology on the origins of eusociality. We made detailed study of the ecology of three gall-dwelling species that show clear differences in their levels of social behaviour. To elucidate evolutionary relationships and to attempt to estimate the number of origins of sociality, we also created a phylogeny based on sequences spanning the mitochondrial genes Cytochrome Oxidase I and II for nine species of Pemphigus.     

Genetic differentiation across the social transition in a socially polymorphic sweat bee,Halictus rubicundus

Eusociality is widely considered a major evolutionary transition. The socially polymorphic sweat bee Halictus rubicundus, solitary in cooler regions of its Holarctic range and eusocial in warmer parts, is an excellent model organism to address this transition, and specifically the question of whether sociality is associated with a strong barrier to gene flow between phenotypically divergent populations. Mitochondrial DNA (COI) from specimens collected across the British Isles, where both solitary and social phenotypes are represented, displayed limited variation, but placed all specimens in the same European lineage; haplotype network analysis failed to differentiate solitary and social lineages. Microsatellite genetic variability was high and enabled us to quantify genetic differentiation among populations and social phenotypes across Great Britain and Ireland. Results from conceptually different analyses consistently showed greater genetic differentiation between geographically distant populations, independently of their social phenotype, suggesting that the two social forms are not reproductively isolated. A landscape genetic approach revealed significant isolation by distance (Mantel test r = 0.622, P < 0.001). The Irish Sea acts as physical barrier to gene flow (partial Mantel test r = 0.453, P < 0.01), indicating that geography, rather than expression of solitary or social behaviour (partial Mantel test r = −0.238, P = 0.053), had a significant effect on the genetic structure of H. rubicundus across the British Isles. Although we cannot reject the hypothesis of a genetic underpinning to differences in solitary and eusocial phenotypes, our data clearly demonstrate a lack of reproductive isolation between the two social forms.