Phylogenetic analysis suggests that sociality is associated with reduced effectiveness of selection

The evolution of sociality in spiders is associated with female bias, reproductive skew and an inbreeding mating system, factors that cause a reduction in effective population size and increase effects of genetic drift. These factors act to decrease the effectiveness of selection, thereby increasing the fixation probability of deleterious mutations. Comparative studies of closely related species with contrasting social traits and mating systems provide the opportunity to test consequences of low effective population size on the effectiveness of selection empirically. We used phylogenetic analyses of three inbred social spider species and seven outcrossing subsocial species of the genus Stegodyphus, and compared dN/dS ratios and codon usage bias between social Inbreeding and subsocial outcrossing mating systems to assess the effectiveness of selection. The overall results do not differ significantly between the social inbreeding and outcrossing species, but suggest a tendency for lower codon usage bias and higher dN/dS ratios in the social inbreeding species compared with their outcrossing congeners. The differences in dN/dS ratio and codon usage bias between social and subsocial species are modest but consistent with theoretical expectations of reduced effectiveness of selection in species with relatively low effective population size. The modest differences are consistent with relatively recent evolution of social mating systems. Additionally, the short terminal branches and lack of speciation of the social lineages, together with low genetic diversity lend support for the transient state of permanent sociality in spiders.     

Evolution of sociality in spiders leads to depleted genomic diversity at both population and species levels

Across several animal taxa, the evolution of sociality involves a suite of characteristics, a “social syndrome,” that includes cooperative breeding, reproductive skew, primary female‐biased sex ratio, and the transition from outcrossing to inbreeding mating system, factors that are expected to reduce effective population size (Ne). This social syndrome may be favoured by short‐term benefits but come with long‐term costs, because the reduction in Ne amplifies loss of genetic diversity by genetic drift, ultimately restricting the potential of populations to respond to environmental change. To investigate the consequences of this social life form on genetic diversity, we used a comparative RAD‐sequencing approach to estimate genomewide diversity in spider species that differ in level of sociality, reproductive skew and mating system. We analysed multiple populations of three independent sister‐species pairs of social inbreeding and subsocial outcrossing Stegodyphus spiders, and a subsocial outgroup. Heterozygosity and within‐population diversity were sixfold to 10‐fold lower in social compared to subsocial species, and demographic modelling revealed a tenfold reduction in Ne of social populations. Species‐wide genetic diversity depends on population divergence and the viability of genetic lineages. Population genomic patterns were consistent with high lineage turnover, which homogenizes the genetic structure that builds up between inbreeding populations, ultimately depleting genetic diversity at the species level. Indeed, species‐wide genetic diversity of social species was 5–8 times lower than that of subsocial species. The repeated evolution of species with this social syndrome is associated with severe loss of genomewide diversity, likely to limit their evolutionary potential.     

Group living and inbreeding depression in a subsocial spider

Social spiders are unusual among social organisms in being highly inbred-males and females mature within their natal nest and mate with each other to produce successive generations. Several lines of evidence suggest that in spiders inbred social species originated from outbred subsocial ancestors, a transition expected to have been hindered by inbreeding depression. As a window into this transition, we examined the fitness consequences of artificially imposed inbreeding in the naturally outbred subsocial spider Anelosimus cf. jucundus. Subsocial spiders alternate periods of solitary and social living and are thought to resemble the ancestral system from which the inbred social species originated. We found that inbreeding depression in this subsocial spider only becomes evident in spiders raised individually following the end of their social phase and that ecological and demographic factors such as eclosion date, number of siblings in the group and mother's persistence are more powerful determinants of fitness during the social phase. A potential explanation for this pattern is that maternal care and group living provide a buffer against inbreeding depression, a possibility that may help explain the repeated origin of inbred social systems in spiders and shed light on the origin of other systems involving regular inbreeding.     

Low genetic diversity and strong but shallow population differentiation suggests genetic homogenization by metapopulation dynamics in a social spider

Mating systems and population dynamics influence genetic diversity and structure. Species that experience inbreeding and limited gene flow are expected to evolve isolated, divergent genetic lineages. Metapopulation dynamics with frequent extinctions and colonizations may, on the other hand, deplete and homogenize genetic variation, if extinction rate is sufficiently high compared to the effect of drift in local demes. We investigated these theoretical predictions empirically in social spiders that are highly inbred. Social spiders show intranest mating, female‐biased sex ratio, and frequent extinction and colonization events, factors that deplete genetic diversity within nests and populations and limit gene flow. We characterized population genetic structure in Stegodyphus sarasinorum, a social spider distributed across the Indian subcontinent. Species‐wide genetic diversity was estimated over approximately 2800 km from Sri Lanka to Himalayas, by sequencing 16 protein‐coding nuclear loci. We found 13 SNPs in 6592 bp (π = 0.00045) indicating low species‐wide nucleotide diversity. Three genetic lineages were strongly differentiated; however, only one fixed difference among them suggests recent divergence. This is consistent with a scenario of metapopulation dynamics that homogenizes genetic diversity across the species' range. Ultimately, low standing genetic variation may hamper a species' ability to track environmental change and render social inbreeding spiders ‘evolutionary dead‐ends’.     

Sociality in theridiid spiders: repeated origins of an evolutionary dead end

Evolutionary "dead ends" result from traits that are selectively advantageous in the short term but ultimately result in lowered diversification rates of lineages. In spiders, 23 species scattered across eight families share a social system in which individuals live in colonies and cooperate in nest maintenance, prey capture, and brood care. Most of these species are inbred and have highly female-biased sex ratios. Here we show that in Theridiidae this social system originated eight to nine times independently among 11 to 12 species for a remarkable 18 to 19 origins across spiders. In Theridiidae, the origins cluster significantly in one clade marked by a possible preadaptation: extended maternal care. In most derivations, sociality is limited to isolated species: social species are sister to social species only thrice. To examine whether sociality in spiders represents an evolutionary dead end, we develop a test that compares the observed phylogenetic isolation of social species to the simulated evolution of social and non-social clades under equal diversification rates, and find that sociality in Theridiidae is significantly isolated. Because social clades are not in general smaller than their nonsocial sister clades, the "spindly" phylogenetic pattern-many tiny replicate social clades-may be explained by extinction rapid enough that a nonsocial sister group does not have time to diversify while the social lineage remains extant. In this case, this repeated origin and extinction of sociality suggests a conflict between the short-term benefits and long-term costs of inbred sociality. Although benefits of group living may initially outweigh costs of inbreeding (hence the replicate origins), in the long run the subdivision of the populations in relatively small and highly inbred colony lineages may result in higher extinction, thus an evolutionary dead end.     

Analysis of the effects of inbreeding on lifespan and starvation resistance in <Emphasis Type="Italic">Drosophila melanogaster</Emphasis>

Because of their decreased overall fitness and genetic variability inbred individuals are expected to show reduced survival and lifespan under most environmental conditions as compared with outbred individuals. Whereas evidence for the deleterious effects of inbreeding on lifespan has been previously provided, only a few studies have investigated effects of inbreeding on survival under starved conditions. In the present study we compared the abilities of inbred and outbred adult Drosophila melanogaster to survive under starved and fed conditions. We found that inbreeding reduced lifespan but had no effect on starvation resistance. The results indicate highly trait specific consequences of inbreeding. Possible mechanisms behind the observed results are discussed.     

Natal Dispersal Patterns of a Subsocial Spider Anelosimus cf. jucundus (Theridiidae)

Species that alternate periods of solitary and social living may provide clues to the conditions that favor sociality. Social spiders probably originated from subsocial‐like ancestors, species in which siblings remain together for part of their life cycle but disperse prior to mating. Exploring the factors that lead to dispersal in subsocial species, but allow the development of large multigenerational colonies in social species, may provide insight into this transition. We studied the natal dispersal patterns of a subsocial spider, Anelosimus cf. jucundus, in Southeastern Arizona. In this population, spiders disperse from their natal nests in their penultimate and antepenultimate instars over a 3‐mo period. We tracked the natal dispersal of marked spiders at sites with clustered vs. isolated nests. We found that most spiders initially dispersed less than 5 m from their natal nests. Males and females, and spiders in patches with different densities of nests, dispersed similar distances. The fact that both sexes in a group dispersed, the lack of a sex difference in dispersal distance, and the relatively short distances dispersed are consistent with the hypothesis that natal dispersal results from resource competition within the natal nest, rather than inbreeding avoidance in competition for mates. Additionally, an increase in the average distance dispersed with time and with the number of spiders leaving a nest suggests that competition for nest sites in the vicinity of the natal nest may affect dispersal distances. The similar distances dispersed in patches with isolated vs. clustered nests, in contrast, suggest that competition among dispersers from different nests may not affect dispersal distances.     

The significance of relatedness and gene flow on population genetic structure in the subsocial spider Eresus cinnaberinus (Araneae: Eresidae)

Interdemic selection, inbreeding and highly structured populations have been invoked to explain the evolution of cooperative social behaviour in the otherwise solitary and cannibalistic spiders. The family Eresidae consists of species ranging from solitary and intermediate subsocial to species exhibiting fully cooperative social behaviour. In this study we, in a hierarchical analysis, investigated relatedness of putative family clusters, inbreeding and population genetic structure of the subsocial spider Eresus cinnaberinus. Five hierarchical levels of investigation ranging from large scale genetic structure (distances of 250 and 50 km level 1 and 2) over microgeographic structure (20 km² and 4 km², level 3 and 4) to a single hill transect of 200 m (level 5) were performed. The purpose of level 5 was two-fold: (1) to investigate the relatedness of putative family groups, and (2) to evaluate the influence of both family living and sampling design on higher level estimates. Relatedness estimates of putative family groups showed an average relatedness of R=0.26. There was no indication of inbreeding. In contrast to social spiders, genetic variation was abundant, H_e?0.10. The population genetic structure was intermediate between social and asocial spiders. Genetic variance increased continually across hierarchical levels. Family structured neighbourhoods biased differentiation estimates among level 5 samples (F_ST? 0.04) and level 3 and 4 samples (0.07ST<0.18), and apparent inbreeding among level 3 and 4 samples, F_IS>0, was caused by disjunct sampling from separate neighbourhoods. Larger scale samples were highly differentiated 0.12ST<0.26, depending on level and sampling design. Due to a distance effect family living did not influence estimates of the higher level 1. Although the dispersing sex among social spiders and the subsocial E. cinnebarinus differ, females versus males, female behaviour of both sociality classes lead to high genetic variance.     

Range‐wide genetic structure of a cooperative mouse in a semi‐arid zone: Evidence for panmixia

Landscape topography and the mobility of individuals will have fundamental impacts on a species’ population structure, for example by enhancing or reducing gene flow and therefore influencing the effective size and genetic diversity of the population. However, social organization will also influence population genetic structure. For example, species that live and breed in cooperative groups may experience high levels of inbreeding and strong genetic drift. The western pebble‐mound mouse (Pseudomys chapmani), which occupies a highly heterogeneous, semi‐arid landscape in Australia, is an enigmatic social mammal that has the intriguing behaviour of working cooperatively in groups to build permanent pebble mounds above a subterranean burrow system. Here, we used both nuclear (microsatellite) and mitochondrial (mtDNA) markers to analyse the range‐wide population structure of western pebble‐mound mice sourced from multiple social groups. We observed high levels of genetic diversity at the broad scale, very weak genetic differentiation at a finer scale and low levels of inbreeding. Our genetic analyses suggest that the western pebble‐mound mouse population is both panmictic and highly viable. We conclude that high genetic connectivity across the complex landscape is a consequence of the species’ ability to permeate their environment, which may be enhanced by “boom‐bust” population dynamics driven by the semi‐arid climate. More broadly, our results highlight the importance of sampling strategies to infer social structure and demonstrate that sociality is an important component of population genetic structure.     

THE QUANTITATIVE AND MOLECULAR GENETIC ARCHITECTURE OF A SUBDIVIDED SPECIES

In an effort to elucidate the evolutionary mechanisms that determine the genetic architecture of a species, we have analyzed 17 populations of the microcrustacean Daphnia pulex for levels of genetic variation at the level of life-history characters and molecular markers in the nuclear and mitochondrial genomes. This species is highly subdivided, with approximately 30% of the variation for nuclear molecular markers and 50% of the variation for mitochondrial markers being distributed among populations. The average level of genetic subdivision for quantitative traits is essentially the same as that for nuclear markers, which superficially suggests that the life-history characters are diverging at the neutral rate. However, the existence of a strong correlation between the levels of population subdivision and broadsense heritabilities of individual traits argues against this interpretation, suggesting instead that the among-population divergence of some quantitative traits (most notably body size) is being driven by local adaptation to different environments. The fact that the mean phenotypes of the individual populations are also strongly correlated with local levels of homozygosity indicates that variation in local inbreeding plays a role in population differentiation. Rather than being a passive consequence of local founder effects, levels of homozygosity may be selected for directly for their effects on the phenotype (adaptive inbreeding depression). There is no relationship between the levels of variation within populations for molecular markers and quantitative characters, and this is explained by the fact that the average standing genetic variation for life-history characters in this species is equivalent to only 33 generations of variation generated by mutation.     

Madagascar: an unexpected hotspot of social Anelosimus spider diversity (Araneae: Theridiidae)

Abstract. The spider genus Anelosimus Simon, 1891 (Theridiidae) currently contains over forty described species, found worldwide in tropical to warm temperate areas. American Anelosimus are all social, a rare trait among spiders, but social behaviour has not been reported for Anelosimus species elsewhere. Old World Anelosimus are poorly known, both behaviourally and taxonomically, and no Anelosimus species have yet been described from sub-Saharan Africa or Madagascar. Based on a preliminary phylogenetic analysis we predicted sociality in an undescribed Madagascar species because it grouped among social New World species. An expedition to Madagascar then found no less than five undescribed periodic-social (subsocial) Anelosimus species in Périnet reserve. A sixth species from the same locality is known from museum specimens and the Anelosimus diversity of Périnet is comparable with the most diverse single locality in the Americas. Subsocial species play a key role in understanding the evolution of permanent sociality (quasisociality). This increased pool of available subsocial study species demonstrates the utility of phylogenies as predictors of traits in species thus far unstudied. Here, A. andasibe sp.n. , A. may Agnarsson sp.n. , A. nazariani sp.n. , A. sallee sp.n. , A. salut sp.n. and A. vondrona sp.n. are described. Anelosimus locketi Roberts, 1977 from Aldabra Atoll is a junior synonym of A. decaryi ( Fage, 1930 ) comb.n. from Madagascar. Preliminary data on the behaviour of the new species are given, indicating a level of sociality similar to the American A.‘arizona’¹. The phylogenetic analysis supports the monophyly of the Madagascar group and places it as sister to a clade containing the eximius lineage from the Americas, and a pair of undescribed Tanzanian species.     

Outbreeding effects in an inbreeding insect,Cimex lectularius

In some species, populations with few founding individuals can be resilient to extreme inbreeding. Inbreeding seems to be the norm in the common bed bug, Cimex lectularius, a flightless insect that, nevertheless, can reach large deme sizes and persist successfully. However, bed bugs can also be dispersed passively by humans, exposing inbred populations to gene flow from genetically distant populations. The introduction of genetic variation through this outbreeding could lead to increased fitness (heterosis) or be costly by causing a loss of local adaptation or exposing genetic incompatibility between populations (outbreeding depression). Here, we addressed how inbreeding within demes and outbreeding between distant populations impact fitness over two generations in this re‐emerging public health pest. We compared fitness traits of families that were inbred (mimicking reproduction following a founder event) or outbred (mimicking reproduction following a gene flow event). We found that outbreeding led to increased starvation resistance compared to inbred families, but this benefit was lost after two generations of outbreeding. No other fitness benefits of outbreeding were observed in either generation, including no differences in fecundity between the two treatments. Resilience to inbreeding is likely to result from the history of small founder events in the bed bug. Outbreeding benefits may only be detectable under stress and when heterozygosity is maximized without disruption of coadaptation. We discuss the consequences of these results both in terms of inbreeding and outbreeding in populations with genetic and spatial structuring, as well as for the recent resurgence of bed bug populations.     

Obligatory female philopatry affects genetic population structure in the ant Proformica longiseta

Evolution of sociality has instigated many changes in the biology of social insects. Particularly, evolution towards complex social systems in ants affects how individuals move in space, usually by making females philopatric. Proformica longisetais well-suited for studying the effects of female philopatry, because female sexuals are wingless and do not actively disperse. We studied genetic population structure in P. longiseta in local scale both as genetic viscosity within one subpopulation, and as differentiation between closely (0.1–1.5 km) located subpopulations, by using nuclear (microsatellites) and mitochondrial (SSCP) markers. Dependent colony founding by splitting old nests is the only known nest founding strategy in P. longiseta. However, no genetic viscosity was detected at the nuclear markers within the subpopulation studied, possibly due to the dynamic nature of P. longiseta populations. The extreme female philopatry showed as strong structure between closely located subpopulations in the mitochondrial genome, but there was no isolation by distance showing that the differentiation pattern was random. Genetic structure in the nuclear genome was much weaker, and there was an indication of isolation by distance. This suggests that male dispersal is strong but not totally free across the area. Finally, non-dispersing P. longiseta females necessarily mate locally raising the possibility of inbreeding, but inbreeding coefficients showed that mating is random. Received 10 January 2006; revised 13 April 2006; accepted 20 April 2006.     

The susceptibility and response of inbred and outbred Mimulus guttatus to infection by Cucumber mosaic virus

The deleterious effects of inbreeding have been well documented, but only recently have studies begun to explore the consequences of inbreeding for important ecological interactions. We examined the effects of inbreeding on the interaction between host and pathogen using the mixed-mating Mimulus guttatus (Scrophulariaceae) and Cucumber mosaic virus (CMV). Inbred (self) and outbred M. guttatus from two California populations (M5 and M13) were rub-inoculated with CMV and compared to sham-inoculated controls. Flower production by outbred plants in host population M5 showed little effect of the inoculation treatment, but inoculation reduced flower production of inbred plants by 12%, indicating that inbreeding reduces tolerance to CMV infection. This interaction fell short of significance, however. The effects of inbreeding and CMV inoculation on biomass in M5 varied significantly across the 15 families used in this experiment, indicating genetic variation in the effect of inbreeding on resistance or tolerance to CMV. CMV infection reduced biomass in host population M13, but there were no significant interactions between virus treatment and level of inbreeding for either flower production or biomass. Enzyme linked immunosorbent assay (ELISA) was used to detect CMV in host tissues. In both populations, mean ELISA absorbance values of inoculated plants were nearly identical for self and outcross hosts, indicating equal susceptibility to CMV. In outbred plants of population M5, flower production did not change with increasing ELISA absorbance, but in inbred plants it declined, indicating reduced tolerance to CMV infection. The results from this study suggest that pathogens may become increasingly detrimental as host populations become more inbred.     

Inbreeding depression in ring-tailed lemurs (<Emphasis Type="Italic">Lemur catta</Emphasis>): genetic diversity predicts parasitism,immunocompetence, and survivorship

The consequences of inbreeding have been well studied in a variety of taxa, revealing that inbreeding has major negative impacts in numerous species, both in captivity and in the wild; however, as trans-generational health data are difficult to obtain for long-lived, free-ranging species, similar analyses are generally lacking for nonhuman primates. Here, we examined the long-term effects of inbreeding on numerous health estimates in a captive colony of ring-tailed lemurs (Lemur catta), housed under semi-natural conditions. This vulnerable strepsirrhine primate is endemic to Madagascar, a threatened hotspot of biodiversity; consequently, this captive population represents an important surrogate. Despite significant attention to maintaining the genetic diversity of captive animals, breeding colonies invariably suffer from various degrees of inbreeding. We used neutral heterozygosity as an estimate of inbreeding and showed that our results reflect genome-wide inbreeding, rather than local genetic effects. In particular, we found that genetic diversity affects several fitness correlates, including the prevalence and burden of Cuterebra parasites and a third (N = 6) of the blood parameters analyzed, some of which reflect immunocompetence. As a final validation of inbreeding depression in this captive colony, we showed that, compared to outbred individuals, inbred lemurs were more likely to die earlier from diseases. Through these analyses, we highlight the importance of monitoring genetic variation in captive animals—a key objective for conservation geneticists—and provide insight into the potential negative consequences faced by small or isolated populations in the wild. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Fine‐scale genetic structure reflects sex‐specific dispersal strategies in a population of sociable weavers (Philetairus socius)

Dispersal is a critical driver of gene flow, with important consequences for population genetic structure, social interactions and other biological processes. Limited dispersal may result in kin‐structured populations in which kin selection may operate, but it may also increase the risk of kin competition and inbreeding. Here, we use a combination of long‐term field data and molecular genetics to examine dispersal patterns and their consequences for the population genetics of a highly social bird, the sociable weaver (Philetairus socius), which exhibits cooperation at various levels of sociality from nuclear family groups to its unique communal nests. Using 20 years of data, involving capture of 6508 birds and 3151 recaptures at 48 colonies, we found that both sexes exhibit philopatry and that any dispersal occurs over relatively short distances. Dispersal is female‐biased, with females dispersing earlier, further, and to less closely related destination colonies than males. Genotyping data from 30 colonies showed that this pattern of dispersal is reflected by fine‐scale genetic structure for both sexes, revealed by isolation by distance in terms of genetic relatedness and significant genetic variance among colonies. Both relationships were stronger among males than females. Crucially, significant relatedness extended beyond the level of the colony for both sexes. Such fine‐scale population genetic structure may have played an important role in the evolution of cooperative behaviour in this species, but it may also result in a significant inbreeding risk, against which female‐biased dispersal alone is unlikely to be an effective strategy.     

The effects of inbreeding, genetic dissimilarity and phenotype on male reproductive success in a dioecious plant

Pollen fate can strongly affect the genetic structure of populations with restricted gene flow and significant inbreeding risk. We established an experimental population of inbred and outbred Silene latifolia plants to evaluate the effects of (i) inbreeding depression, (ii) phenotypic variation and (iii) relatedness between mates on male fitness under natural pollination. Paternity analysis revealed that outbred males sired significantly more offspring than inbred males. Independently of the effects of inbreeding, male fitness depended on several male traits, including a sexually dimorphic (flower number) and a gametophytic trait (in vitro pollen germination rate). In addition, full-sib matings were less frequent than randomly expected. Thus, inbreeding, phenotype and genetic dissimilarity simultaneously affect male fitness in this animal-pollinated plant. While inbreeding depression might threaten population persistence, the deficiency of effective matings between sibs and the higher fitness of outbred males will reduce its occurrence and counter genetic erosion.     

Influence of volcanic activity on the population genetic structure of Hawaiian Tetragnatha spiders: fragmentation, rapid population growth and the potential for accelerated evolution

Volcanic activity on the island of Hawaii results in a cyclical pattern of habitat destruction and fragmentation by lava, followed by habitat regeneration on newly formed substrates. While this pattern has been hypothesized to promote the diversification of Hawaiian lineages, there have been few attempts to link geological processes to measurable changes in population structure. We investigated the genetic structure of three species of Hawaiian spiders in forests fragmented by a 150-year-old lava flow on Mauna Loa Volcano, island of Hawaii: Tetragnatha quasimodo (forest and lava flow generalist), T. anuenue and T. brevignatha (forest specialists). To estimate fragmentation effects on population subdivision in each species, we examined variation in mitochondrial and nuclear genomes (DNA sequences and allozymes, respectively). Population subdivision was higher for forest specialists than for the generalist in fragments separated by lava. Patterns of mtDNA sequence evolution also revealed that forest specialists have undergone rapid expansion, while the generalist has experienced more gradual population growth. Results confirm that patterns of neutral genetic variation reflect patterns of volcanic activity in some Tetragnatha species. Our study further suggests that population subdivision and expansion can occur across small spatial and temporal scales, which may facilitate the rapid spread of new character states, leading to speciation as hypothesized by H. L. Carson 30 years ago.     

The genetic rescue of two bottlenecked South Island robin populations using translocations of inbred donors

Populations forced through bottlenecks typically lose genetic variation and exhibit inbreeding depression. ‘Genetic rescue’ techniques that introduce individuals from outbred populations can be highly effective in reversing the deleterious effects of inbreeding, but have limited application for the majority of endangered species, which survive only in a few bottlenecked populations. We tested the effectiveness of using highly inbred populations as donors to rescue two isolated and bottlenecked populations of the South Island robin (Petroica australis). Reciprocal translocations significantly increased heterozygosity and allelic diversity. Increased genetic diversity was accompanied by increased juvenile survival and recruitment, sperm quality, and immunocompetence of hybrid individuals (crosses between the two populations) compared with inbred control individuals (crosses within each population). Our results confirm that the implementation of ‘genetic rescue’ using bottlenecked populations as donors provides a way of preserving endangered species and restoring their viability when outbred donor populations no longer exist.