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Abstract

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 genome-wide 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 6-10 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 genome-wide diversity, likely to limit their evolutionary potential. This article is protected by copyright. All rights reserved.

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... Spider sociality has a twiggy phylogenetic distribution, where the closest relatives of most social species are not social 21-24 . By comparing pairs of social species and their closest nonsocial (i.e., subsocial) relatives within a single genus, recent studies have begun to identify the genetic consequences of spider sociality and associated shifts from outbreeding to inbreeding 23,[26][27][28][29] . These studies, together with a preliminary comparative genomic study of two social species from one genus and several solitary species 30 , have begun to identify putative genomic signatures of the evolution of sociality in spiders, including elevated genome-wide rates of molecular evolution 26-30 . ...
... Spider sociality has a twiggy phylogenetic distribution, where the closest relatives of most social species are not social [21][22][23][24] . By comparing pairs of social species and their closest nonsocial (i.e., subsocial) relatives within a single genus, recent studies have begun to identify the genetic consequences of spider sociality and associated shifts from outbreeding to inbreeding 23,[26][27][28][29] . These studies, together with a preliminary comparative genomic study of two social species from one genus and several solitary species 30 , have begun to identify putative genomic signatures of the evolution of sociality in spiders, including elevated genome-wide rates of molecular evolution [26][27][28][29][30] . ...
... By comparing pairs of social species and their closest nonsocial (i.e., subsocial) relatives within a single genus, recent studies have begun to identify the genetic consequences of spider sociality and associated shifts from outbreeding to inbreeding 23,[26][27][28][29] . These studies, together with a preliminary comparative genomic study of two social species from one genus and several solitary species 30 , have begun to identify putative genomic signatures of the evolution of sociality in spiders, including elevated genome-wide rates of molecular evolution [26][27][28][29][30] . ...
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The transition from solitary to social life is a major phenotypic innovation, but its genetic underpinnings are largely unknown. To identify genomic changes associated with this transition, we compare the genomes of 22 spider species representing eight recent and independent origins of sociality. Hundreds of genes tend to experience shifts in selection during the repeated transition to social life. These genes are associated with several key functions, such as neurogenesis, behavior, and metabolism, and include genes that previously have been implicated in animal social behavior and human behavioral disorders. In addition, social species have elevated genome-wide rates of molecular evolution associated with relaxed selection caused by reduced effective population size. Altogether, our study provides unprecedented insights into the genomic signatures of social evolution and the specific genetic changes that repeatedly underpin the evolution of sociality. Our study also highlights the heretofore unappreciated potential of transcriptomics using ethanol-preserved specimens for comparative genomics and phylotranscriptomics.
... These spiders, referred to as social or cooperatively breeding spiders, are similar to other cooperatively breeding animals, such as lions and meerkats, in that adults cooperate in caring for colony offspring, and group members forage and feed together Grinsted & Lubin 2019). Although sociality in spiders is phylogenetically rare, this behavior has evolved convergently multiple times within several spider genera (Agnarsson et al. 2006;Aviles & Guevara 2017;Settepani et al. 2017). While all social spiders display similar cooperative, behavioral traits, we have limited knowledge on whether cooperative strategies in relation to group hunting differ among species. ...
... Cooperative foraging in spiders is most frequently studied in the genera Stegodyphus (Eresidae) and Anelosimus Simon, 1891 (Theridiidae) (Aviles & Guevara 2017). Both genera contain a number of social species that have evolved independently from an ancestral subsocial state (Agnarsson et al. 2006;Settepani et al. 2017). Subsocial spiders show extended maternal care by sharing prey with or regurgitating food for their offspring, and juveniles have a temporary cooperative stage within their maternal nest after their mother has died, after which they disperse to live and breed solitarily (Yip & Rayor 2014). ...
... Subsocial spiders show extended maternal care by sharing prey with or regurgitating food for their offspring, and juveniles have a temporary cooperative stage within their maternal nest after their mother has died, after which they disperse to live and breed solitarily (Yip & Rayor 2014). In all fully social, cooperatively breeding spiders, the dispersal stage prior to mating has been lost entirely, leading to siblings reproducing within colonies, and an obligate inbreeding mating system (Settepani et al. 2017). In Stegodyphus, three species are social while the remaining species are subsocial (Kraus & Kraus 1988). ...
Article
Sociality in spiders has evolved independently multiple times, resulting in convergently evolved cooperative breeding and prey capture. In all social spiders, prey is captured by only a subset of group members and then shared with other, non-attacking group members. However, spiders' propensity to attack prey may differ among species due to species-specific trade-offs between risks, costs and benefits of prey capture involvement. We explored whether engagement in prey attack differs among three social Stegodyphus species, using orthopteran prey, and found substantial differences. Stegodyphus mimosarum Pavesi, 1883 had a low prey acceptance rate, was slow to attack prey, and engaged very few spiders in prey attack. In S. sarasinorum Karsch, 1892, prey acceptance was high, independently of prey size, but more spiders attacked when prey was small. While medium-sized prey had higher acceptance rate in S. dumicola Pocock, 1898, indicating a preference, the number of attackers was not affected by prey size. Our results suggest that the three species may have different cooperative prey capture strategies. In S. mimosarum and S. dumicola, whose geographical ranges overlap, these strategies may represent niche specialization, depending on whether their respective cautious and choosy approaches extend to other prey types than orthopterans, while S. sarasinorum may have a more opportunistic approach. We discuss factors that can affect social spiders' foraging strategy, such as prey availability, predation pressure, and efficiency of the communal web to ensnare prey. Future studies are required to investigate to which extent species-specific cooperative foraging strategies are shaped by ontogeny, group size, and plastic responses to environmental factors.
... Groups of closely related spiders live in communal nests containing tens to hundreds of individuals (Avilés 1997), who collaborate on reproduction, brood care, and foraging (Lubin and Bilde 2007 (Crouch and Lubin 2001;Bilde et al. 2007). Notably, there is no pre-mating dispersal, and reproduction therefore occurs among highly related offspring, which leads to a strictly inbreeding mating system (Settepani et al. 2017). The combination of a strict inbreeding ...
... mating system, female-biased sex ratio, and frequent extinction-colonization events has severe consequences for population genetic diversity and structure: genetic diversity is extremely low within populations, and despite restricted gene flow between populations, population extinctionrecolonization causes remarkably low genetic divergence among populations (Lubin and Bilde 2007;Vanthournout et al. 2018;Settepani et al. 2014Settepani et al. , 2017Bechsgaard et al. 2019). This type of host metapopulation dynamics may have implications for host-microbiome dynamics (Mihaljevic 2012;Miller et al. 2018), but potentially also for the spatial distribution of the microbiome composition. ...
... In contrast to the finding of clear temporal stability in nest microbiome composition, we document substantially higher dissimilarity between nests found in close proximity (within populations, Fig. 3). This is interesting, given the spiders' high genetic similarity between nests (Lubin and Bilde 2007;Settepani et al. 2017) and the similar environmental and climatic conditions within a population. We suggest that the founding of new nests offers opportunities for shifts in microbiome composition. ...
Article
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Host symbiont interactions may form obligatory or facultative associations that are context dependent. Long-term studies on microbiome composition from wild populations should assess the temporal and spatial dynamics of host-microbe associations. We characterized the temporal and spatial variation in the bacterial microbiome composition in six populations of the social spider Stegodyphus dumicola for 2.5 years, using 16S rRNA gene amplicon sequencing of whole spiders. Individuals within a nest exhibit highly similar microbiomes, which remain stable over several generations and are not predictably affected by seasonal variation in temperature or humidity. This stability in nest microbiome is likely due to social transmission, whereas drift-like processes during new nest foundations explain variation in host microbiomes between nests. This is supported by the lack of obligate symbionts (i.e. no symbionts are present in all spider individuals). Quantitative PCR analyses showed that the bacterial load of individual spiders is stable in healthy nests but can increase dramatically in perishing nests. These increases are not driven by specific bacterial taxa but likely caused by loss of host immune control under deteriorating conditions. Spider nests show an annual survival rate of approximately 45%, but nest death is not correlated to microbiome composition, and the bacteria found in S. dumicola are not considered to be high virulence pathogens.
... We sampled 10 adult crickets from each of the 11 populations sam- Raw read processing was done as in Settepani et al. (2017) to obtain data for further analyses. In brief, raw reads (forward and reverse) ...
... In those cases, we used the forward read for further analyses if it passed quality filtering. See Settepani et al. (2017) for further details. ...
... We used pyRAD v2.15 (steps 3-7) (Eaton, 2014) to analyse RAD tag data using the following parameter settings: 'clustering thresh- We used Python scripts, also adapted from Settepani et al. (2017) to further process the output of the pyRAD analyses to estimate nucleotide diversity (π) (Tajima, 1983) and genetic structure. To perform population genetic analyses, it was necessary to remove any bias arising from the difference in RAD loci length. ...
Article
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Understanding how species can thrive in a range of environments is a central challenge for evolutionary ecology. There is strong evidence for local adaptation along large‐scale ecological clines in insects. However, potential adaptation among neighbouring populations differing in their environment has been studied much less. We used RAD‐sequencing to quantify genetic divergence and clustering of ten populations of the field cricket Gryllus campestris in the Cantabrian Mountains of northern Spain, and an outgroup on the coastal plain. Our populations were chosen to represent replicate high and low altitude habitats. We identified genetic clusters that include both high and low altitude populations indicating that the two habitat types do not hold ancestrally distinct lineages. Using common‐garden rearing experiments to remove environmental effects, we found evidence for differences between high and low altitude populations in physiological and life‐history traits. As predicted by the local adaptation hypothesis, crickets with parents from cooler (high altitude) populations recovered from periods of extreme cooling more rapidly than those with parents from warmer (low altitude) populations. Growth rates also differed between offspring from high and low altitude populations. However, contrary to our prediction that crickets from high altitudes would grow faster, the most striking difference was that at high temperatures, growth was fastest in individuals from low altitudes. Our findings reveal that populations a few tens of kilometres apart have independently evolved adaptations to their environment. This suggests that local adaptation in a range of traits may be commonplace even in mobile invertebrates at scales of a small fraction of species’ distributions.
... The spider genus Stegodyphus (family Eresidae) contains three species (S. sarasinorum, S. mimosarum, and S. dumicola), that show extraordinarily low genetic diversity as consequence of an independently evolved, yet highly similar social lifestyle ( Figure 1A; Johannesen et al., 2007;Settepani et al., 2016Settepani et al., , 2017. These spiders live in nests of 100-1000 of individuals (typically 85% female) and cooperate on web building, prey capture, feeding, and brood care . ...
... In both cases, new nests are established by females who were already mated in their natal nest, allowing propagation of their family lineage with no genetic mixing (Schneider et al., 2001). Nests belonging to the same population are highly related and likely stem from a single mated ballooning female and subsequent nest-fissions (Settepani et al., 2017). ...
... The combination of female-biased sex ratio, reproductive skew, and inbreeding ("social syndrome") leads to enhanced genetic drift causing very low levels of genetic diversity within spider nests and populations (Settepani et al., 2017). ...
Article
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Social spiders have remarkably low species-wide genetic diversities, potentially increasing the relative importance of microbial symbionts for host fitness. Here we explore the bacterial microbiomes of three species of social Stegodyphus (S. dumicola, S. mimosarum, and S. sarasinorum), within and between populations, using 16S rRNA gene amplicon sequencing. The microbiomes of the three spider species were distinct but shared similarities in membership and structure. This included low overall diversity (Shannon index 0.5–1.7), strong dominance of single symbionts in individual spiders (McNaughton’s dominance index 0.68–0.93), and a core microbiome (>50% prevalence) consisting of 5–7 specific symbionts. The most abundant and prevalent symbionts were classified as Chlamydiales, Borrelia, and Mycoplasma, all representing novel, presumably Stegodyphus-specific lineages. Borrelia- and Mycoplasma-like symbionts were localized by fluorescence in situ hybridization (FISH) in the spider midgut. The microbiomes of individual spiders were highly similar within nests but often very different between nests from the same population, with only the microbiome of S. sarasinorum consistently reflecting host population structure. The weak population pattern in microbiome composition renders microbiome-facilitated local adaptation unlikely. However, the retention of specific symbionts across populations and species may indicate a recurrent acquisition from environmental vectors or an essential symbiotic contribution to spider phenotype.
... Although multiple factors have likely selected for sociality in spiders, such as eliminating the high mortality associated with dispersal and solitary living, and benefitting from increased survival and growth rates of juveniles due to cooperative breeding (Aviles and Tufino 1998;Bilde et al. 2007;Settepani et al. 2017), the access to large prey is likely to play a role at least in facilitating the evolution of spider sociality (Aviles and Guevara 2017;Majer et al. 2018Majer et al. , 2015Majer et al. , 2013a. The link between sociality and prey size is well documented and extensively researched within spiders of the genus Anelosimus (Theridiidae). ...
... The genus consists of > 20 species of which the majority are subsocial. The three cooperatively breeding species have independently evolved sociality, and each social species has a subsocial species as its sister species (Johannesen et al. 2007;Settepani et al. 2017). For this study, we collected data on the acceptance of prey of various sizes on all three social species (S. dumicola, S. mimosarum, and S. sarasinorum) and three subsocial species (S. lineatus, S. pacificus, and S. tibialis). ...
... We used the most recent partial phylogeny of Stegodyphus published in Settepani et al. (2017) (provided by J. Bechsgaard). For Anelosimus, we used the most recent partial phylogeny (generously provided by I. Agnarsson, unpublished data). ...
Article
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One of the benefits of cooperative hunting may be that predators can subdue larger prey. In spiders, cooperative, social species can capture prey many times larger than an individual predator. However, we propose that cooperative prey capture does not have to be associated with larger caught prey per se, but with an increase in the ratio of prey to predator body size. This can be achieved either by catching larger prey while keeping predator body size constant, or by evolving a smaller predator body size while maintaining capture of large prey. We show that within a genus of relatively large spiders, Stegodyphus, subsocial spiders representing the ancestral state of social species are capable of catching the largest prey available in the environment. Hence, within this genus, the evolution of cooperation would not provide access to otherwise inaccessible, large prey. Instead, we show that social Stegodyphus spiders are smaller than their subsocial counterparts, while catching similar sized prey, leading to the predicted increase in prey-predator size ratio with sociality. We further show that in a genus of small spiders, Anelosimus, the level of sociality is associated with an increased size of prey caught while predator size is unaffected by sociality, leading to a similar, predicted increase in prey-predator size ratio. In summary, we find support for our proposed ‘prey to predator size ratio hypothesis’ and discuss how relaxed selection on large body size in the evolution of social, cooperative living may provide adaptive benefits for ancestrally relatively large predators.
... In many cooperative group-living species, individuals are genetically related and engage in helping based on kinship (nepotism), but seek nonkin as mating partners, thereby maintaining an outcrossing mating system (Brouwer, Van De Pol, Atema, & Cockburn, 2011;Keller & Passera, 1993;O'Riain, Bennett, Brotherton, McIlrath, & Clutton-Brock, 2000;Shellman-Reeve, 2001). There are, however, several social taxa that exhibit fully inbred mating systems (overview in Settepani et al., 2017), for example social spiders and bark beetles, in which ecological constraints have led to the elimination of natal dispersal and regular intragroup mating (Berger-Tal, Tuni, Lubin, Smith, & Bilde, 2014;Bilde et al., 2005;Peer & Taborsky, 2005). These species with a history of inbreeding may experience increased tolerance to inbreeding through purging (Bilde et al., 2005;Charlesworth & Charlesworth, 1987;Crnokrak et al., 2002). ...
... Social spiders of the genus Stegodyphus provide an ideal model for exploring whether active mate choice for related individuals occurs in the context of inbreeding tolerance, as this is a species with an inbreeding mating system and low genetic diversity within populations (Settepani et al., 2017). Social Stegodyphus species cooperate in various activities such as web building, brood care and foraging (Lubin & Bilde, 2007). ...
... Owing to a lack of premating dispersal, mating occurs among closely related individuals within the group (Lubin & Bilde, 2007), and new nests are established by a single female and her offspring, thus propagating an inbred lineage (Johannesen, Hennig, Dommermuth, & Schneider, 2002). These lineages are genetically similar, and overall population-and species-wide genetic diversity is extraordinarily low due to low effective population size and genetic homogenization by frequent extinction -colonization events (Johannesen, Wickler, Seibt, & Moritz, 2009;Lubin & Bilde, 2007;Settepani, Bechsgaard, & Bilde, 2014;Settepani et al., 2017;Smith, Van Rijn, Henschel, Bilde, & Lubin, 2009). Phylogenetic analyses support the notion that social spiders evolved from subsocial species (species with extended maternal care) through the elimination of premating dispersal. ...
Article
Mate preference based on relatedness may evolve in response to costs and benefits of inbreeding avoidance. Whereas mating with closely related individuals can have negative fitness consequences due to inbreeding depression, it may simultaneously be favoured by inclusive fitness benefits. Variation in the fitness payoff shaped by benefits of inbreeding may even lead to preference for mating with kin. We investigated this hypothesis in the social spider Stegodyphus dumicola, a cooperative species in which reproduction occurs among siblings within the group, premating dispersal is lacking and infrequent encounters with unrelated individuals result in homozygous genetic lineages. We tested whether female mate choice is influenced by male relatedness by pairing females with males that differ in the degree of genetic relatedness, namely nest members, non-nest members from the same population and non-nest members from allopatric populations. We recorded premating (male rejections, latency to mating) and mating (copulation duration and interruptions) behaviours. Females showed no preference for partners on the basis of their relatedness during the premating phase, as frequencies of rejections and successful matings did not differ markedly in encounters with nest and non-nest members. This suggests that selection on discriminatory mechanisms may be weakened or lost in species with inbreeding tolerance and in which relatedness between interacting individuals is very high and variance in relatedness extremely low. Unrelated males from the geographically distant population experienced longer copu- lations than males from the same population. We interpret this finding as depicting a possible scenario of a between-population reproductive barrier or functional incompatibility, which may be the mechanism causing lower fitness in between-population crosses previously documented in these populations.
... Comparisons of closely related species have proven useful for elucidating genetic consequences of biological differences, because of their recently shared evolutionary history (Cutter et al. 2008;Guo et al. 2009;Settepani et al. 2017). Here, we present a study of two sister species with contrasting mating systems from the spider genus Stegodyphus: the subsocial outcrossing species S. africanus and its social inbreeding sister species S. mimosarum, with the subsocial outcrossing S. lineatus as an outgroup ( fig. 1) (Johannesen et al. 2007;Settepani et al. 2016). ...
... Stegodyphus spiders have an X0 sex determining system, where females have two copies of two X chromosomes (X 1 X 2 /X 1 X 2 ) and males have one copy of the two X chromosomes (X 1 X 2 /0) (Forman M, personal communication). Differences in their degree of sociality and mating system, and associated life histories and population dynamics, are expected to influence substitution and diversity patterns of X chromosomes and autosomes differently: The subsocial outbreeding S. africanus has an equal primary sex ratio (Vanthournout et al. 2018), and populations are expected to be relatively stable in sizes and existence over evolutionary time Settepani et al. 2017). In contrast, the social obligatory inbreeding S. mimosarum shows a highly female-biased primary sex ratio , caused by male production of a higher proportion of X 1 X 2 -containing sperm cells than sperm cells without X chromosomes (Vanthournout et al. 2018). ...
... In contrast, the social obligatory inbreeding S. mimosarum shows a highly female-biased primary sex ratio , caused by male production of a higher proportion of X 1 X 2 -containing sperm cells than sperm cells without X chromosomes (Vanthournout et al. 2018). Furthermore, empirical data suggest that population extinction rates in social Stegodyphus species such as S. mimosarum are high (Crouch and Lubin 2001;Bilde et al. 2007), implying a high rate of population colonization ), a pattern supported by recent population genomic analyses (Settepani et al. 2017). Differences in sex ratio influence the relative effective population sizes of X chromosomes and autosomes. ...
Article
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In species with chromosomal sex determination, X chromosomes are predicted to evolve faster than autosomes because of positive selection on recessive alleles or weak purifying selection. We investigated X chromosome evolution in Stegodyphus spiders that differ in mating system, sex-ratio, and population dynamics. We assigned scaffolds to X chromosomes and autosomes using a novel method based on flow cytometry of sperm cells and reduced representation sequencing. We estimated coding substitution patterns (dN/dS) in a subsocial outcrossing species (S. africanus) and its social inbreeding and female biased sister species (S. mimosarum), and found evidence for faster-X evolution in both species. X chromosome to autosome diversity (piX/piA) ratios were estimated in multiple populations. The average piX/piA estimates of S. africanus (0.57 (95% CI: 0.55-0.60)), was lower than the neutral expectation of 0.75, consistent with more hitchhiking events on X-linked loci and/or a lower X chromosome mutation rate, and we provide evidence in support of both. The social species S. mimosarum has a significantly higher piX/piA ratio (0.72 (95% CI: 0.65-0.79) in agreement with its female biased sex ratio. Stegodyphus mimosarum also have different piX/piA estimates among populations, which we interpret as evidence for recurrent founder events. Simulations show that recurrent founder events are expected to decrease the piX/piA estimates in S. mimosarum, thus underestimating the true effect of female biased sex ratios. Finally, we found lower synonymous divergence on X chromosomes in both species, and the male-to-female substitution ratio to be higher than 1, indicating a higher mutation rate in males.
... The three species share some common characteristics such as inbreeding, a female biased sex ratio, and strong extinction/recolonization dynamics [22,23]. These traits cause an extremely low species-wide genetic diversity within species [24,25]. Particularly, S. dumicola has one of the lowest genetic diversities estimated in any species studied so far [25,26]. ...
... These traits cause an extremely low species-wide genetic diversity within species [24,25]. Particularly, S. dumicola has one of the lowest genetic diversities estimated in any species studied so far [25,26]. ...
... To generate the WG-PB data, we first extracted genomic DNA from the pool of 50 individuals from a single nest. We note that intra-colony genetic diversity is extremely low in S. dumicola [25], so nucleotide diversity, copy number, and structural variation should not influence the genome assembly. The spiders were flash frozen in liquid nitrogen and ground to a powder before adding 10 mL of extraction buffer (10 mM Tris pH 8, 100 mM EDTA, 0.02 mg RNase/mL buffer, 0.5% SDS). ...
Article
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Variation in DNA methylation patterns among genes, individuals, and populations appears to be highly variable among taxa, but our understanding of the functional significance of this variation is still incomplete. We here present the first whole genome bisulfite sequencing of a chelicerate species, the social spider Stegodyphus dumicola. We show that DNA methylation occurs mainly in CpG context and is concentrated in genes. This is a pattern also documented in other invertebrates. We present RNA sequence data to investigate the role of DNA methylation in gene regulation and show that, within individuals, methylated genes are more expressed than genes that are not methylated and that methylated genes are more stably expressed across individuals than unmethylated genes. Although no causal association is shown, this lends support for the implication of DNA CpG methylation in regulating gene expression in invertebrates. Differential DNA methylation between populations showed a small but significant correlation with differential gene expression. This is consistent with a possible role of DNA methylation in local adaptation. Based on indirect inference of the presence and pattern of DNA methylation in chelicerate species whose genomes have been sequenced, we performed a comparative phylogenetic analysis. We found strong evidence for exon DNA methylation in the horseshoe crab Limulus polyphemus and in all spider and scorpion species, while most Parasitiformes and Acariformes species seem to have lost DNA methylation.
... Sociality has evolved independently at least 20 times in seven spider families, and phylogenetic patterns suggest that it is derived from a subsocial state (Agnarsson, Avil es, Coddington, & Maddison, 2006;Settepani, Bechsgaard, & Bilde, 2016), by elimination of premating dispersal and the formation of family groups. Mating and reproduction take place in the nest among related group members, which results in extreme inbreeding and high genetic relatedness (Agnarsson, Avil es, & Maddison, 2013;Settepani, Bechsgaard, & Bilde, 2014;Settepani et al., 2017). Social spider species show a strong female-biased sex ratio; however, only a small proportion of females reproduce (Avil es, 1997;Salomon, Mayntz, & Lubin, 2008). ...
... In S. dumicola, a large proportion of females remain unmated (Salomon et al., 2008), and their engagement in allomaternal care must enhance the growth and survival of the offspring in the nest. In return, these virgin females gain considerable inclusive fitness benefits because of the high genetic relatedness among individuals in the nest Settepani et al., 2017). The physiological ability of virgins to provide extreme brood care may also provide assurance against the death of reproductive females (Schneider & Lubin, 1997). ...
... This behavioural differentiation, together with recent evidence for individual specialization (Settepani et al., 2013;Pruitt & Riechert, 2011;Wright et al., 2014), suggests a more complex social organization in social spiders than previously recognized. Because relatedness within the nest is extremely high Settepani et al., 2017), the nest represents the reproductive unit, and fitness is defined by nest productivity and not solely by individual reproductive success (Boomsma, 2009;Keller, 1999). High intranest relatedness should reduce conflict over reproduction because indirect fitness of helpers will be similar to direct fitness, thereby aligning the interests of individuals. ...
Article
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Division of reproductive behaviour and alloparental care are key aspects of many animal societies. In cooperatively breeding species, variation in helping effort and unequal task participation are frequently observed. However, the extent to which the reproductive state of an individual affects the tasks performed during offspring care remains poorly understood. In the social spider Stegodyphus dumicola, approximately 40% of females reproduce, and mothers show extended maternal care including eggsac tending, regurgitation feeding and matriphagy, in which they are consumed by the offspring. We asked whether and to what extent virgin females participate in extreme maternal care and whether they differ from reproducing females in foraging activity. We show that virgin females contributed to all aspects of extended brood care, including regurgitation feeding and matriphagy. This suggests a physiological adaptation in virgin females to cooperative breeding, since in the subsocial Stegodyphus lineatus only mated females provide extended maternal care. Although virgin females and mothers are behaviourally totipotent, we found evidence for task differentiation as virgins engaged less in brood care and more in prey attack than mothers. High relatedness among nestmates and low probability of future reproduction in virgin helpers suggest alignment of reproductive interests between mothers and allomothers. Therefore, extreme allomaternal care by virgin helpers can be considered an adaptation to cooperative breeding in social spiders.
... Inbreeding and stochastic spatially structured buildup of mutation and drift load and resulting asynchronous local population extinctions consequently emerge as properties of the model. Highly structured and inbred systems have arisen multiple times across the animal and plant kingdom (Avilés and Purcell 2012;Settepani et al. 2017). The most prominent and studied example is the frequent evolution of selfing mating systems in plants (Wright et al. 2013). ...
... This effect had already been shown for neutral genetic variation (Slatkin 1977;Wade and McCauley 1988), and here we show it applies also to the genetic load. Our results therefore illustrate how the extremely low levels of genetic diversity observed in systems such as S. dumicola (Johannesen et al. 2007;Leffler et al. 2012;Settepani et al. 2016Settepani et al. , 2017 may result from metapopulation dynamics characterized by local extinctions followed by rapid recolonization events (Settepani et al. 2014), such that most of the metapopulation shares a quite recent coalescent event. ...
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Understanding how genetic and ecological effects can interact to shape genetic loads within and across local populations is key to understanding ongoing persistence of systems that should otherwise be susceptible to extinction through mutational meltdown. Classic theory predicts short persistence times for metapopulations comprising small local populations with low connectivity, due to accumulation of deleterious mutations. Yet, some such systems have persisted over evolutionary time, implying the existence of mechanisms that allow metapopulations to avoid mutational meltdown. We first hypothesize a mechanism by which the combination of stochasticity in the numbers and types of mutations arising locally (genetic stochasticity), resulting local extinction, and recolonization through evolving dispersal, facilitates metapopulation persistence. We then test this mechanism using a spatially and genetically explicit individual‐based model. We show that genetic stochasticity in highly structured metapopulations can result in local extinctions, which can favour increased dispersal, thus allowing recolonization of empty habitat patches. This causes fluctuations in metapopulation size and transient gene flow, which reduces genetic load and increases metapopulation persistence over evolutionary time. Our suggested mechanism and simulation results provide an explanation for the conundrum presented by the continued persistence of highly structured populations with inbreeding mating systems which occur in diverse taxa. This article is protected by copyright. All rights reserved
... Social spiders of the genus Stegodyphus (Eresidae) live in communal nests with up to hundreds of individuals (Avilés, 1997;Lubin and Bilde, 2007). As individuals within nests originate from the same family and reproduce with each other, populations are highly inbred and harbor extremely low genetic diversity, which is hypothesized to limit evolutionary potential (Settepani et al., 2017). Nevertheless, social spiders such as Stegodyphus dumicola Pocock 1898 are widely distributed in (sub)tropical arid regions that encompass multiple climate zones (Kraus and Kraus, 1988;Majer et al., 2013). ...
... We found that the sampled spiders formed three genetically separated populations, but note that this is based on relatively few genetic variants. A previous study demonstrated very low species-level genetic diversity in S. dumicola (Settepani et al., 2017). The different populations had distinct metabolite profiles, but the topology of the phylogenetic tree was not reflected in the metabolite profiles, i.e., the closest related populations, Otavi and Stampriet, had the least similar metabolite profiles. ...
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Animals experience climatic variation in their natural habitats, which may lead to variation in phenotypic responses among populations through local adaptation or phenotypic plasticity. In ectotherm arthropods, the expression of thermoprotective metabolites such as free amino acids, sugars, and polyols, in response to temperature stress, may facilitate temperature tolerance by regulating cellular homeostasis. If populations experience differences in temperatures, individuals may exhibit population-specific metabolite profiles through differential accumulation of metabolites that facilitate thermal tolerance. Such thermoprotective metabolites may originate from the animals themselves or from their associated microbiome, and hence microbial symbionts may contribute to shape the thermal niche of their host. The social spider Stegodyphus dumicola has extremely low genetic diversity, yet it occupies a relatively broad temperature range occurring across multiple climate zones in Southern Africa. We investigated whether the metabolome, including thermoprotective metabolites, differs between populations, and whether population genetic structure or the spider microbiome may explain potential differences. To address these questions, we assessed metabolite profiles, phylogenetic relationships, and microbiomes in three natural populations along a temperature gradient. The spider microbiomes in three genetically distinct populations of S. dumicola showed no significant population-specific pattern, and none of its dominating genera (Borrelia, Diplorickettsia, and Mycoplasma) are known to facilitate thermal tolerance in hosts. These results do not support a role of the microbiome in shaping the thermal niche of S. dumicola. Metabolite profiles of the three spider populations were significantly different. The variation was driven by multiple metabolites that can be linked to temperature stress (e.g., lactate, succinate, or xanthine) and thermal tolerance (e.g., polyols, trehalose, or glycerol): these metabolites had higher relative abundance in spiders from the hottest geographic region. These distinct metabolite profiles are consistent with a potential role of the metabolome in temperature response.
... The social lifestyle in spiders comes with elimination of pre-mating dispersal and therefore a strictly inbreeding mating system. Combined with frequent extinction and colonization events, this results in extremely low genetic diversity (Lubin and Bilde, 2007;Settepani et al., 2014Settepani et al., , 2016Settepani et al., , 2017. Homozygosity in genes within individuals, and low population genetic diversity in for example immune genes is likely to be associated with elevated vulnerability to infections. ...
... Thus, the lowest number of VOCs was found at the highest altitude (Windhoek). In contrast to the spider microbiome, it was shown that S. dumicola shows little genetic differences between sampling sites (Settepani et al., 2017), which makes the spiders themselves very unlikely as an influencing factor for the differences between locations. Even though most of the VOCs were not shared between the sampling sites, some VOCs were present at all sites which suggests a site-independent "core volatilome" of S. dumicola. ...
Article
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Social arthropods such as termites, ants, and bees are among others the most successful animal groups on earth. However, social arthropods face an elevated risk of infections due to the dense colony structure, which facilitates pathogen transmission. An interesting hypothesis is that social arthropods are protected by chemical compounds produced by the arthropods themselves, microbial symbionts, or plants they associate with. Stegodyphus dumicola is an African social spider species, inhabiting communal silk nests. Because of the complex three-dimensional structure of the spider nest antimicrobial volatile organic compounds (VOCs) are a promising protection against pathogens, because of their ability to diffuse through air-filled pores. We analyzed the volatilomes of S. dumicola, their nests, and capture webs in three locations in Namibia and assessed their antimicrobial potential. Volatilomes were collected using polydimethylsiloxane (PDMS) tubes and analyzed using GC/Q-TOF. We showed the presence of 199 VOCs and tentatively identified 53 VOCs. More than 40% of the tentatively identified VOCs are known for their antimicrobial activity. Here, six VOCs were confirmed by analyzing pure compounds namely acetophenone, 1,3-benzothiazole, 1-decanal, 2-decanone, 1-tetradecene, and docosane and for five of these compounds the antimicrobial activity were proven. The nest and web volatilomes had many VOCs in common, whereas the spider volatilomes were more differentiated. Clear differences were identified between the volatilomes from the different sampling sites which is likely justified by differences in the microbiomes of the spiders and nests, the plants, and the different climatic conditions. The results indicate the potential relevance of the volatilomes for the ecological success of S. dumicola.
... Previous studies of spider social evolution have been mostly limited to behavioral and ecological aspects, and emphasize the importance of food supply (Bilde & Lubin, 2001;Rypstra, 1983Rypstra, , 1986Whitehouse & Lubin, 2005) in group formation. However, the genetic changes involved in the transition from solitary to group-living are yet to be concluded (Settepani et al., 2017;Tong et al., 2020). We suggest that group-living evolution in spiders is related to nutrient metabolism and ...
... Although displaying similar group-living behaviors, permanent aggregation and suppressed cannibalism, cooperative and colonial spiders have different effective population sizes. Cooperative spiders are inbred and show depleted genomic diversity (Settepani et al., 2017), while the colonial species have outbred population structures like solitary species. Thus, in cooperative and colonial spiders, the effectiveness of selection or selection response will differ even under similar group-living selection intensities. ...
Article
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Although widely thought to be aggressive, solitary, and potentially cannibalistic, some spider species have evolved group-living behaviors. The distinct transition provides the framework to uncover group-living evolution. Here, we conducted a comparative transcriptomic study and examined patterns of molecular evolution in two independently evolved group-living spiders and twelve solitary species. We report that positively selected genes among group-living spider lineages are significantly enriched in nutrient metabolism and autophagy pathways. We also show that nutrient-related genes of group-living spiders convergently experience amino acid substitutions and accelerated relative evolutionary rates. These results indicate adaptive convergence of nutrient metabolism that may ensure energy supply in group-living spiders. The decelerated evolutionary rate of autophagy-related genes in group-living lineages is consistent with an increased constraint on energy homeostasis as would be required in a group-living environment. Together, the results show that energy metabolic pathways play an important role in the transition to group-living in spiders. 蜘蛛普遍被认为具攻击性、独居、潜在同类相食,但是部分蜘蛛进化出了群居的行为。基于比较转录组研究,发现群居蜘蛛受到正选择基因富集在营养代谢和自噬通路上。结果表明能量代谢通路在改变蜘蛛从攻击性到社会性中的作用。
... Among these, double-digest RADseq, or ddRAD-seq (Peterson et al. 2012), is highly customizable as regards to the final number of loci, according to the choice of enzymes and range of fragment sizes selected. The ddRAD-seq approach has been applied with success to many purposes including population genetic studies (Kjeldsen et al. 2016;Black et al. 2017;Sherpa et al. 2018a, b;Capblancq et al. 2019), phylogenetic reconstructions (DaCosta and Sorenson, 2016;Vargas et al. 2017;Boubli et al. 2018;Lee et al. 2018;Sherpa et al. 2018a, b), demographic inferences (Capblancq et al. 2015;Nunziata et al. 2017;Settepani et al. 2017;Elleouet and Aitken 2018) and landscape genetic analyses (Saenz-Agudelo et al. 2015;Johnson et al. 2017;Capblancq et al. 2020). Despite the recognized advantages of the ddRAD-seq technique, several limitations and weaknesses are highlighted in the literature (Davey et al. 2013;Andrews et al. 2016;Lowry et al. 2017). ...
... To estimate the influence of the m and M values on loci recovery, we determined the number of reconstructed loci, their mean coverage and the proportion of polymorphic loci for each value of M and m tested. We also evaluated the impact of these parameters on population genetics results by performing, for all m and M values, some of the most commonly used analyses using ddRAD-seq data (Capblancq et al. 2015;Kjeldsen et al. 2016;Black et al. 2017;Nunziata et al. 2017;Settepani et al. 2017;Elleouet and Aitken 2018;Sherpa et al. 2018a, b), i.e., mean individual heterozygosity, F ST among populations estimated with the adegenet R package (Jombart 2008), Principal Component Analysis (PCA) using the adegenet R package (Jombart 2008), genetic structure with sNMF using the LEA R package (Frichot and François 2015), and evolutionary history reconstruction using Approximate Bayesian Computation, performed with the diyABC program (Cornuet et al. 2014). The ABC analyses were conducted using a different evolutionary scenario for each model: hybrid speciation for the Coenonympha model and population divergence for the Fagus model. ...
Article
Full-text available
Next-generation sequencing technologies have opened a new era of research in population genetics. Following these new sequencing opportunities, the use of restriction enzyme-based genotyping techniques, such as restriction site-associated DNA sequencing (RAD-seq) or double-digest RAD-sequencing (ddRAD-seq), has dramatically increased in the last decade. From DNA sampling to SNP calling, the laboratory and bioinformatic parameters of enzyme-based techniques have been investigated in the literature. However, the impact of those parameters on downstream analyses and biological results remains less documented. In this study, we investigated the effects of sevral pre- and post-sequencing settings on ddRAD-seq results for two biological systems: a complex of butterfly species (Coenonympha sp.) and several populations of common beech (Fagus sylvatica). Our results suggest that pre-sequencing parameters (i.e., DNA quantity, number of PCR cycles during library preparation) have a significant impact on the number of recovered reads and SNPs, on the number of unique alleles and on individual heterozygosity. In the same way, we found that post-sequencing settings (i.e., clustering and minimum coverage thresholds) influenced loci reconstruction (e.g., number of loci, mean coverage) and SNP calling (e.g., number of SNPs; heterozygosity) but had only a marginal impact on downstream analyses (e.g., measure of genetic differentiation, estimation of individual admixture, and demographic inferences). In addition, replication analyses confirmed the reproducibility of the ddRAD-seq procedure. Overall, this study assesses the degree of sensitivity of ddRAD-seq data to pre- and post-sequencing protocols, and illustrates its robustness when studying population genetics.
... Together, these form the 'lost colulus clade', which is ancestrally reconstructed to display extensive maternal care and construct three-dimensional webs (Agnarsson, 2004), both putative pre-adaptations to sociality in spiders (Avilés, 1997;Bilde & Lubin, 2011;Yip & Rayor, 2014). In both subsocial and social spider species of this clade, cooperative groups are made up of close kin, typically a single matriline (Avilés, 1997;Agnarsson et al., 2010Agnarsson et al., , 2013Avilés & Guevara, 2017;Settepani et al., 2017;Viera & Agnarsson, 2017). ...
... In this scenario, we would expect males to disperse among colonies/areas to secure gene flow and thus avoid inbreeding, leading to deep mitochondrial but limited nuclear DNA genetic structuring. Interestingly, social spiders lack a pre-mating dispersal stage for both males and females and therefore have extraordinarily high levels of inbreeding (Settepani et al., 2017), whereas both sexes in colonial spiders are expected to maintain relatively high levels of dispersal (Johannesen et al., 2012). The results from our molecular study indicate that females might have severely limited dispersal in these two Chikunia species. ...
Article
Group-living behaviour is rare in spiders but has evolved repeatedly, yielding several species, some showing cooperation among close kin, and others living in colonies where each female builds its own web and is territorial. The most frequent origins of group living are seen in the cobweb spiders (Theridiidae) that commonly build three-dimensional webs and show extensive maternal care, both putatively pre-adaptive traits to spider sociality. A very unusual behaviour was recently discovered in the theridiid genus Chikunia, where two distinct but related species occur in mixed-species colonies with potentially indiscriminate brood care. These mixed colonies consist of Chikunia nigra and a newly discovered species. Here, we describe the new species, Chikunia bilde sp. nov., and summarize the unique biology of this species pair. We also place the origin of mixed-species group living in a phylogenetic context, firmly confirming the placement of Chikunia within the clade (lost colulus clade) previously characterized as containing a concentration of independent origins of group living. The two Chikunia studied here are sister species, representing a rare case of close genetic and behavioural interspecific relationship. We conclude that the loss of aggression that accompanies group living and social behaviour in cobweb spiders might help to explain the origin of mixed-species colonies.
... The resulting marker density has greatly contributed to an in-depth understanding of evolutionary and ecological processes, including in the field of arachnology (Brewer et al. 2014). Several spider genomes have recently been sequenced (Sanggaard et al. 2014;Babb et al. 2017;Schwager et al. 2017), the spider tree of life has been tackled using high-density markers (Bond et al. 2014;Ferna´ndez et al. 2014Ferna´ndez et al. , 2018 and genomic and transcriptomic analyses have provided insights into evolutionary divergence in spiders (Croucher et al. 2013;Bechsgaard et al. 2015;Krehenwinkel et al. 2015;Settepani et al. 2017). The recent isolation of Ultra Conserved Elements ) and application of ddRAD (double digest) sequencing protocols (Burns et al. 2017;Settepani et al. 2017) have additionally contributed a wealth of genetic markers for spider research. ...
... Several spider genomes have recently been sequenced (Sanggaard et al. 2014;Babb et al. 2017;Schwager et al. 2017), the spider tree of life has been tackled using high-density markers (Bond et al. 2014;Ferna´ndez et al. 2014Ferna´ndez et al. , 2018 and genomic and transcriptomic analyses have provided insights into evolutionary divergence in spiders (Croucher et al. 2013;Bechsgaard et al. 2015;Krehenwinkel et al. 2015;Settepani et al. 2017). The recent isolation of Ultra Conserved Elements ) and application of ddRAD (double digest) sequencing protocols (Burns et al. 2017;Settepani et al. 2017) have additionally contributed a wealth of genetic markers for spider research. However, RAD sequencing (Burns et al. 2017) or sequence capture (Smith et al. 2013;Cotoras et al. 2018) protocols are relatively laborious and expensive and the analysis of such high throughput genotyping data requires considerable computational resources. ...
Article
Full-text available
High throughput sequencing (HTS) has emerged as a valuable tool for the rapid isolation of genetic markers for population genetics and pedigree analysis. HTS-based SNP (single nucleotide polymorphism) genotyping protocols like RAD (Restriction-site associated DNA) sequencing or hybrid capture allow for the isolation of thousands of markers from any non-model organism. However, these protocols are relatively laborious and expensive and the resulting high marker density is not always necessary. Since HTS technology has also greatly simplified the process of microsatellite marker isolation and genotyping, we develop microsatellite markers as a cost-efficient and simple alternative to SNP genotyping. We present low coverage genome sequencing data from seven distantly related spider species (Argiope bruennichi (Scopoli, and show the utility of HTS for microsatellite isolation. We also present a simple Illumina amplicon sequencing protocol to genotype microsatellites from multiplex PCR amplicons in the Hawaiian happy face spider T. grallator. We discuss advantages and drawbacks of the use of microsatellites for a range of research questions, and highlight an unexpectedly fast decay and gain of repeat loci for T. grallator.
... Together, these form the 'lost colulus clade', which is ancestrally reconstructed to display extensive maternal care and construct three-dimensional webs (Agnarsson, 2004), both putative pre-adaptations to sociality in spiders (Avilés, 1997;Bilde & Lubin, 2011;Yip & Rayor, 2014). In both subsocial and social spider species of this clade, cooperative groups are made up of close kin, typically a single matriline (Avilés, 1997;Agnarsson et al., 2010Agnarsson et al., , 2013Avilés & Guevara, 2017;Settepani et al., 2017;Viera & Agnarsson, 2017). ...
... In this scenario, we would expect males to disperse among colonies/areas to secure gene flow and thus avoid inbreeding, leading to deep mitochondrial but limited nuclear DNA genetic structuring. Interestingly, social spiders lack a pre-mating dispersal stage for both males and females and therefore have extraordinarily high levels of inbreeding (Settepani et al., 2017), whereas both sexes in colonial spiders are expected to maintain relatively high levels of dispersal (Johannesen et al., 2012). The results from our molecular study indicate that females might have severely limited dispersal in these two Chikunia species. ...
Article
Full-text available
Group-living behaviour is rare in spiders but has evolved repeatedly, yielding several species, some showing cooperation among close kin, and others living in colonies where each female builds its own web and is territorial. The most frequent origins of group living are seen in the cobweb spiders (Theridiidae) that commonly build three-dimensional webs and show extensive maternal care, both putatively pre-adaptive traits to spider sociality. A very unusual behaviour was recently discovered in the theridiid genus Chikunia, where two distinct but related species occur in mixed-species colonies with potentially indiscriminate brood care. These mixed colonies consist of Chikunia nigra and a newly discovered species. Here, we describe the new species, Chikunia bilde sp. nov., and summarize the unique biology of this species pair. We also place the origin of mixed-species group living in a phylogenetic context, firmly confirming the placement of Chikunia within the clade (lost colulus clade) previously characterized as containing a concentration of independent origins of group living. The two Chikunia studied here are sister species, representing a rare case of close genetic and behavioural interspecific relationship. We conclude that the loss of aggression that accompanies group living and social behaviour in cobweb spiders might help to explain the origin of mixed-species colonies.
... The genetic diversity at the species-level was 5-8 times lower in social species than in their subsocial sister species, and heterozygosity and diversity within populations were 6-10 times lower in the social compared to the subsocial species. Furthermore, populations were much more genetically structured and differentiated in the social species, with F st values more than 10 times lower in subsocial than social species (Settepani et al., 2017). ...
... In the case of social spiders, the rarity of sociality in the spider phylogeny suggest that the barriers to evolving the social syndrome are not easily overcome, and once attained, the social syndrome is resistant to further change. The loss of genetic diversity through repeated inbreeding likely makes sociality an 'evolutionary dead end': Despite short-term benefits to a cooperative lifestyle longterm costs include an inability to adapt to a changing environment, and loss of the potential to diversify and speciate (Agnarsson et al., 2006;Settepani et al., 2017). How some social species are capable of inhabiting geographical areas of widely different environmental conditions, despite a depletion of genetic variability at the species level, is still an intriguing mystery. ...
Chapter
Group living, social behavior and cooperative breeding has evolved multiple times in spiders, although only very few spider species permanently live in groups. Here, we give a brief overview of the two types of permanent group living in spiders and the evolutionary pathways leading to social and colonial living in spiders.
... A striking example of CSD species with highly femalebiased sex ratio is found in social spiders, which are cooperative breeders that live in permanent groups with an obligatory inbreeding mating system [17][18][19][20]. Social spider groups are usually composed of around 85% females [17], and female bias is considered adaptive by reducing competition for fertilization between brothers (local mate competition [5]) and/or increasing the number of females as the helping sex (local resource enhancement [2,4,6,21,22]). ...
... inbreeding mating system and as a consequence, extraordinary high homozygosity and almost no genetic variation [20]. This social spider system can, therefore, be viewed as an extended version of the local mate competition model that predicts increased allocation to daughters, to reduce competition between highly related males within the nest over access to females over multiple generations (haystack model) [2,19,59]. ...
Article
Sex allocation theory predicts that when sons and daughters have different reproductive values, parents should adjust offspring sex ratio towards the sex with the higher fitness return. Haplo-diploid species directly control offspring sex ratio, but species with chromosomal sex determination (CSD) were presumed to be constrained by Mendelian segregation. There is now increasing evidence that CSD species can adjust sex ratio strategically, but the underlying mechanism is not well understood. One hypothesis states that adaptive control is more likely to evolve in the heterogametic sex through a bias in gamete production. We investigated this hypothesis in males as the heterogametic sex in two social spider species that consistently show adaptive female-biased sex ratio and in one subsocial species that is characterized by equal sex ratio. We quantified the production of male (0) and female (X) determining sperm cells using flow cytometry, and show that males of social species produce significantly more X-carrying sperm than 0-sperm, on average 70%. This is consistent with the production of more daughters. Males of the subsocial species produced a significantly lower bias of 54% X-carrying sperm. We also investigated whether inter-genomic conflict between hosts and their endosymbionts may explain female bias. Next generation sequencing showed that five common genera of bacterial endosymbionts known to affect sex ratio are largely absent, ruling out that endosymbiont bacteria bias sex ratio in social spiders. Our study provides evidence for paternal control over sex allocation through biased gamete production as a mechanism by which the heterogametic sex in CSD species adaptively adjust offspring sex ratio.
... The genus Stegodyphus was divided into three groups africanus, dufouri and mirandus, based on differences in the genitalia of both sexes -each containing one social and several subsocial species (Kraus and Kraus, 1989). Molecular phylogenetic analysis confirmed the groups (Johannesen et al., 2007;Settepani et al., 2017), but showed that the subsocial S. lineatus can be considered sister group to all other Stegodyphus species (Settepani et al., 2017). Consequently, S. lineatus and other Eresidae have been used in comparative studies to try to understand the evolution of sociality (Kullmann, 1968;Lubin and Bilde, 2007). ...
... The genus Stegodyphus was divided into three groups africanus, dufouri and mirandus, based on differences in the genitalia of both sexes -each containing one social and several subsocial species (Kraus and Kraus, 1989). Molecular phylogenetic analysis confirmed the groups (Johannesen et al., 2007;Settepani et al., 2017), but showed that the subsocial S. lineatus can be considered sister group to all other Stegodyphus species (Settepani et al., 2017). Consequently, S. lineatus and other Eresidae have been used in comparative studies to try to understand the evolution of sociality (Kullmann, 1968;Lubin and Bilde, 2007). ...
Article
The anatomy of the female genitalia sets the arena for sperm competition in species in which females mate multiply and store sperm. In spiders, females possess cuticular internal structures that have evolved into diverse sperm storage sites. Here, we investigate the female genital morphology of seven eresid spider species. We used X-ray micro-computed tomography for 3D reconstruction of the anatomy of the female genital system in the social Stegodyphus dumicola, S. mimosarum and S. sarasinorum, and the subsocial S lineatus, S. pacificus, S. tentoriicola as well as Eresus sandaliatus. We used histology to assess the sites of sperm storage in two selected species S. lineatus and S. dumicola. Our results show that the internal genitalia of the Stegodyphus species consist of two bilateral folds instead of closed ducts as often reported for entelegyne spiders. Along each fold, three regions are discriminable that differ in their specific morphology but are all surrounded by glandular tissue. Between species, the regions differ in shape and dimension. In virgin females, the lumina of all regions are filled with secretion. In mated females, spermatozoa were found in all three regions; however, only those sperm that are stored in the posterior region seem to become activated. Sperm found in anterior regions are embedded in a substance that might act as a mating plug. Our data suggest that the regions of the female genital tract differ in accessibility by the male as well as in their potential use for ejection and manipulation of sperm by the female.
... RAD methods do not require previous taxon-specific information, imply relatively simple wet-lab work, routinely produce tens of thousands of loci per sample instead of hundreds to a few thousand, and are more cost-effective to implement than transcriptomics or target capture techniques. Whereas multiple spider studies have used RAD-seq for assessing population genomics, phylogeographic and species delimitation questions (Graham et al., 2020;Hedin et al., 2020;Ivanov et al., 2018;Ortiz et al., 2021;Settepani et al., 2017), to the best of our knowledge, only Girard et al. (2021) have used it for reconstructing genus-level phylogenetic relationships, obtaining overwhelmingly high support at all divergence levels for 48 species of peacock spiders of the genus Maratus (Salticidae) plus outgroups. ...
Article
RAD sequencing yields large amounts of genome-wide data at a relatively low cost and without requiring previous taxon-specific information, making it ideal for evolutionary studies of highly diversified and neglected organisms. However, concerns about information decay with phylogenetic distance have discouraged its use for assessing supraspecific relationships. Here, using Double Digest Restriction Associated DNA (ddRAD) data, we perform the first deep-level approach to the phylogeny of Zodarion, a highly diversified spider genus. We explore the impact of loci and taxon filtering across concatenated and multispecies coalescent reconstruction methods and investigate the patterns of information dropout in reference to both the time of divergence and the mitochondrial divergence between taxa. We found that relaxed loci-filtering and nested taxon-filtering strategies maximized the amount of molecular information and improved phylogenetic inference. As expected, there was a clear pattern of allele dropout towards deeper time and mitochondrial divergences, but the phylogenetic signal remained strong throughout the phylogeny. Therefore, we inferred topologies that were almost fully resolved, highly supported, and noticeably congruent between setups and inference methods, which highlights overall inconsistency in the taxonomy of Zodarion. Because Zodarion appears to be among the oldest and most mitochondrially diversified spider genera, our results suggest that ddRAD data show high potential for inferring intra-generic relationships across spiders and probably also in other taxonomic groups.
... Therefore, any animal personality would be expected to manifest in behaviours in this juvenile stage if it is to play a role in task participation, given that individuals moult 12 times before reaching adulthood. These spiders are also highly inbred due to their reduced dispersal potential (Settepani et al., 2017;Smith & Engel, 1994), possibly because of which colonies have highly female-biased sex ratios (Avilés, 1997). ...
Article
Full-text available
Animal personalities and behavioural syndromes have overarching implications for in�dividual survival, fitness and cooperative task participation. In social spiders, person�ality in boldness and aggression, and their association into behavioural syndromes, are thought to play a role in individual participation and task specialisation in collective behaviours, such as prey capture. However, recent retractions of key publications in this field have exposed gaps and uncertainties in our understanding of factors govern�ing task performance in social spider colonies. Here, we analyse an already-published data set on animal personalities in the Indian social spider Stegodyphus sarasinorum to investigate whether boldness and aggression form a behavioural syndrome and assess its persistence over the short- and long-term, and across age classes. Boldness and aggression were negatively correlated traits, forming a syndrome, but only over the long-term in subadult spiders, and not over the short-term in subadults or in juveniles. These results provide evidence for the existence of a behavioural syndrome in at least one social spider species. However, more work is now required to fully understand the observed inconsistencies in behavioural syndrome structures and animal person�alities, as well as their possible role(s) in mediating task partitioning and collective performance in social spider colonies.
... Within the nests, spiders cooperate in various activities such as building capture webs and capturing prey, maintaining the nest, and taking care of brood (Lubin and Bilde 2007). A key characteristic of social spiders is their extremely low species-wide genetic diversity caused by a permanent inbreeding mating system, female-biased sex-ratio, and reproductive skew (Lubin and Bilde 2007;Settepani et al. 2017). The inbreeding mating system of social spiders is thought to have short-term advantages and more fatal long-term consequences, leading to high risks of colony extinction due to a reduced ability to respond to pathogens and other environmental challenges (Agnarsson et al. 2013;Smith et al. 2016). ...
Article
Full-text available
Some social arthropods engage in mutualistic symbiosis with antimicrobial compound-producing microorganisms that provide protection against pathogens. Social spiders live in communal nests and contain specific endosymbionts with unknown function. Bacteria are also found on the spiders’ surface, including prevalent staphylococci, which may have protective potential. Here we present the genomic and phenotypic characterization of strain i1, isolated from the surface of the social spider Stegodyphus dumicola. Phylogenomic analysis identified i1 as novel strain of Staphylococcus sciuri within subgroup 2 of three newly defined genomic subgroups. Further phenotypic investigations showed that S. sciuri i1 is an extremophile that can grow at a broad range of temperatures (4 °C–45 °C), high salt concentrations (up to 27%), and has antimicrobial activity against closely related species. We identified a lactococcin 972-like bacteriocin gene cluster, likely responsible for the antimicrobial activity, and found it conserved in two of the three subgroups of S. sciuri. These features indicate that S. sciuri i1, though not a specific symbiont, is well-adapted to survive on the surface of social spiders and may gain a competitive advantage by inhibiting closely related species.
... Within the nests, spiders cooperate in various activities such as building capture webs and capturing prey, maintaining the nest, and taking care of brood (Lubin and Bilde, 2007). A key characteristic of social spiders is their extremely low species-wide genetic diversity caused by a permanent inbreeding mating system, female-biased sex-ratio, and reproductive skew (Lubin and Bilde, 2007;Settepani et al., 2017). The inbreeding mating system of social spiders is thought to have shortterm advantages and more fatal long-term consequences, leading to high risks of colony extinction due to a reduced ability to respond to pathogens and other environmental challenges (Agnarsson et al., 2013;Smith et al., 2016). ...
Preprint
Full-text available
Some social arthropods engage in mutualistic symbiosis with antimicrobial compound-producing microorganisms that provide protection against pathogens. Social spiders live in communal nests and contain specific endosymbionts with unknown function. Bacteria are also found on the spiders' surface, including prevalent staphylococci, which may have protective potential. Here we present the genomic and phenotypic characterization of strain i1, isolated from the surface of the social spider Stegodyphus dumicola. Phylogenomic analysis identified i1 as novel strain of Staphylococcus sciuri within subgroup 2 of three newly defined genomic subgroups. Further phenotypic investigations showed that S. sciuri i1 is an extremophile that can grow at a broad range of temperatures (4°C-45°C), high salt concentrations (up to 27%), and has antimicrobial activity against closely related species. We identified a lactococcin 972-like bacteriocin gene cluster, likely responsible for the antimicrobial activity, and found it conserved in two of the three subgroups of S. sciuri. These features indicate that S. sciuri i1, though not a specific symbiont, is well-adapted to survive on the surface of social spiders and may gain a competitive advantage by inhibiting closely related species.
... Therefore, the effective population size (N e ) is essentially reduced to the small subset of the population (i.e., the queens) that contributes to breeding. Indeed, sociality is shown to be associated with reduced N e in Hymenoptera (Romiguier et al. 2014;Weyna and Romiguier 2020) and spiders (Settepani et al. 2017). Similarly, in Synalpheus shrimps, demographic inference found lower and more stable N e in eusocial species across the four independent origins of eusociality (Chak, Solomon T. C. Harris, Stephen E. Duffy, J. Emmett Hultgren, Kristin M. Rubenstein, Dustin R., submitted). ...
Article
Full-text available
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 non-eusocial 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.
... Colonies typically reside in a single retreat; however, groups can build multiple nests connected by capture webs. Stegodyphus dumicola colonies are characterized by low dispersal, serial inbreeding, and low within-colony genetic variation Smith et al. 2009;Avilés and Purcell 2012;Settepani et al. 2017). Colony prey capture success is influenced by the scaffolds on which colonies build their webs. ...
Article
Animals often face conflicting demands when making movement decisions. To examine the decision process of social animals, we evaluated nest-site preferences of the social spider Stegodyphus dumicola. Colonies engage in collective web building, constructing 3D nests and 2D capture webs on trees and fences. We examined how individuals and groups decide where to construct a nest based on habitat structure and conspecific presence. Individuals had a strong preference for 3D substrates and conspecific presence. Groups were then provided with conflicting options of 3D substrates versus 2D substrates with a conspecific. Groups preferred the 3D structures without presettled conspecifics over a 2D substrate with conspecifics. When a group fragmented and individuals settled on both substrates, the minority group eventually joined the majority. Before rejoining, the collective prey capture behavior of divided groups improved with the size of the majority fragment. The costs of slow responses to prey for split groups and weak conspecific attraction may explain why dispersal is rare in these spiders.
... Males mate with their sisters leading to high degrees of inbreeding. However, males also show short distance dispersal and enter other colonies (Aviles and Purcell 2012; Settepani et al. 2017;Smith et al. 2016;Lubin et al. 2009;Smith et al. 2016) thus causing gene flow between colonies. While we can directly observe dispersal in large adult Stegodyphus, sex differences in species with juvenile dispersal can only be inferred from population genetic studies that cannot easily differentiate between sex-specific dispersal behavior and sex-specific mortality during dispersal. ...
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Sexual reproduction is pervasive in animals and has led to the evolution of sexual dimorphism. In most animals, males and females show marked differences in primary and secondary sexual traits. The formation of sex-specific organs and eventually sex-specific behaviors is defined during the development of an organism. Sex determination processes have been extensively studied in a few well-established model organisms. While some key molecular regulators are conserved across animals, the initiation of sex determination is highly diverse. To reveal the mechanisms underlying the development of sexual dimorphism and to identify the evolutionary forces driving the evolution of different sexes, sex determination mechanisms must thus be studied in detail in many different animal species beyond the typical model systems. In this perspective article, we argue that spiders represent an excellent group of animals in which to study sex determination mechanisms. We show that spiders are sexually dimorphic in various morphological, behavioral, and life history traits. The availability of an increasing number of genomic and transcriptomic resources and functional tools provides a great starting point to scrutinize the extensive sexual dimorphism present in spiders on a mechanistic level. We provide an overview of the current knowledge of sex determination in spiders and propose approaches to reveal the molecular and genetic underpinnings of sexual dimorphism in these exciting animals.
... Relaxed purifying selection is expected to be especially common in species with low effective population size (N e ), and social species such as social spiders are expected to experience low N e as a result of reproductive skew, female-biased sex ratios, and inbreeding (Romiguier et al. 2014;Settepani et al. 2016;Galtier et al. 2018). Indeed, previous studies in social spiders (Settepani et al. 2014(Settepani et al. , 2016(Settepani et al. , 2017Bechsgaard et al. 2019) and also social insects have found evidence for low N e and genomewide relaxed purifying selection when compared with solitary species (Romiguier et al. 2014;Kapheim et al. 2015;Galtier et al. 2018). Future studies using both polymorphism data and divergence data will be necessary to further tease apart the contribution of elevated positive selection and relaxed purifying selection (Yang and Bielawski 2000;Nielsen 2005) to spider genome evolution. ...
Article
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Comparative genomics has begun to elucidate the genomic basis of social life in insects but insight into the genomic basis of spider sociality has lagged behind. To begin to characterize genomic signatures associated with the evolution of social life in spiders, we performed one of the first spider comparative genomics studies including five solitary species and two social species, representing two independent origins of sociality in the genus Stegodyphus. We found that the two social spider species had a large expansion of gene families associated with transport and metabolic processes and an elevated genome-wide rate of molecular evolution compared with the five solitary spider species. Genes that were rapidly evolving in the two social species relative to the five solitary species were enriched for transport, behavior, and immune functions, while genes that were rapidly evolving in the solitary species were enriched for energy metabolism processes. Most rapidly evolving genes in the social species S. dumicola were broadly expressed across four tissues and enriched for transport functions, but 12 rapidly evolving genes showed brain-specific expression and were enriched for social behavioral processes. Altogether, our study identifies putative genomic signatures and potential candidate genes associated with spider sociality. These results indicate that future spider comparative genomic studies, including broader sampling and additional independent origins of sociality, can further clarify the genomic causes and consequences of social life.
... Several hypotheses have been proposed to explain the high incidence of colony extinction events in social spiders. First, the transition to sociality in spiders is met with a transition from outbreeding to inbreeding, which results in low effective population sizes and a reduced ability to response to changing environmental pressures (Agnarsson et al. 2006, Settepani et al. 2017. Second, the evolution of sociality is associated with a decrease in cross-contextual aggressiveness (e.g., towards conspecifics, heterospecifics, prey, and potential predators/parasites) and increased conspecific densities that together render social spiders susceptible to a diversity of ecological pressures . ...
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Many animal societies are susceptible to mass mortality events and collapse. Elucidating how environmental pressures determine patterns of collapse is important for understanding how such societies function and evolve. Using the social spider Stegodyphus dumicola, we investigated the environmental drivers of colony extinction along two precipitation gradients across southern Africa, using the Namib and Kalahari deserts versus wetter savanna habitats to the north and east. We deployed experimental colonies (n = 242) along two ~ 800-km transects and returned to assess colony success in the field after 2 months. Specifically, we noted colony extinction events after the 2-month duration and collected environmental data on the correlates of those extinction events (e.g., evidence of ant attacks, no. of prey captured). We found that colony extinction events at desert sites were more frequently associated with attacks by predatory ants as compared with savanna sites, while colony extinctions in wetter savannas sites were more tightly associated with fungal outbreaks. Our findings support the hypothesis that environments vary in the selection pressures that they impose on social organisms, which may explain why different social phenotypes are often favored in each habitat. Significance statement Many social animals are susceptible to group extinction events. Identifying the factors that precipitate these events can help us to understand how societies function and evolve. We used a social spider model to evaluate whether the drivers of group extinction events may vary with habitat type. We found that ant attacks were more commonly associated with colony demise at arid sites, whereas fungal outbreaks were associated with collapse in wetter environments. If maintained temporally, these contrasting selection pressures could facilitate the evolution of local adaptation in individual- and colony-level phenotypes and aid in the maintenance of intraspecific trait diversity.
... Research on social spiders has given rise to broad insights about social evolution, sex ratio theory, and animal personality [2, 4, 6-8, 22-24, 39], but they have lagged behind other organisms in the development and application of genomic resources (but see [37,49]). We identify multiple variants in a small genomic region that are strongly associated with boldness in the spider Anelosimus studiosus (Fig. 2), and we develop a preliminary genome assembly and linkage map that will facilitate future genomic studies of this genus (Additional file 1: Figure S1, Tables S2, S3). ...
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Background: Recent research has revealed that polymorphic behavioral strategies shape intra-and interspecific interactions and contribute to fitness in many animal species. A better understanding of the proximate mechanisms underlying these behavioral syndromes will enhance our grasp this phenomenon. Spiders in the genus Anelosimus exhibit inter-individual behavioral variation on several axes: individuals have consistent responses to stimuli (e.g. bold vs. shy individuals) and they are subsocial (exhibiting extended maternal care and sibling cooperation) across most of their range, but they sometimes form permanent social groups in northern temperate regions. Here, we seek genetic variants associated with boldness and with social structure in a socially polymorphic population of the spider Anelosimus studiosus. We also develop preliminary genomic resources, including a genome assembly and linkage map, that support this and future genomic research on this group. Results: Remarkably, we identify a small genomic scaffold (~ 1200 bp) that harbors seven single nucleotide polymorphisms (SNPs) associated with boldness. Moreover, heterozygotes are less common than expected based on Hardy-Weinberg equilibrium, suggesting that either assortative mating or selection against heterozygotes may be occurring in this system. We find no loci significantly associated with social organization. Our draft genome assembly allows us to localize SNPs of interest in this study and to carry out genetic comparisons with other published genomes, although it remains highly fragmented. Conclusions: By identifying a locus associated with a well-studied animal personality trait, this study opens up avenues for future research to link behavioral studies of animal personality with genotype and fitness.
... Relaxed purifying selection is expected to be especially common in species with low effective population size (N e ), and social species such as social spiders are expected to experience low N e as a result of reproductive skew, female-biased sex ratios, and inbreeding (Romiguier et al. 2014;Galtier et al. 2018;Settepani et al. 2016). Indeed, previous studies in social spiders (Settepani et al. 2016;Bechsgaard et al. 2019;Settepani et al. 2017Settepani et al. , 2014 and also social insects have found evidence for low N e and genome-wide relaxed purifying selection when compared to solitary species (Galtier et al. 2018;Kapheim et al. 2015;Romiguier et al. 2014). Future studies using both polymorphism data and divergence data will be necessary to further tease apart the contribution of elevated positive selection and relaxed purifying selection (Yang & Bielawski 2000;Nielsen 2005) to spider genome evolution. ...
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Full-text available
Comparative genomics has begun to elucidate the genomic basis of social life in insects but insight into the genomic basis of spider sociality has lagged behind. To begin to characterize genomic signatures associated with the evolution of social life in spiders, we performed one of the first spider comparative genomics studies including five solitary species and two social species, representing two independent origins of sociality in the genus Stegodyphus. We found that the two social spider species had a large expansion of gene families associated with transport and metabolic processes and an elevated genome-wide rate of molecular evolution compared with the five solitary spider species. Genes that were rapidly evolving in the two social species relative to the five solitary species were enriched for transport, behavior, and immune functions, while genes that were rapidly evolving in the solitary species were enriched for energy metabolism processes. Most rapidly evolving genes in the social species S. dumicola were broadly expressed across four tissues and enriched for transport functions, but 12 rapidly evolving genes showed brain-specific expression and were enriched for social behavioral processes. Altogether, our study identifies putative genomic signatures and potential candidate genes associated with spider sociality. These results indicate that future spider comparative genomic studies, including broader sampling and additional independent origins of sociality, can further clarify the genomic causes and consequences of social life.
... Also unknown are factors and cues that are employed by social spiders in evaluating and settling into a new site during dispersal. Interestingly, the inbreeding coefficients varied in different species of social spiders, with S. sarasinorum showing the lowest value (Settepani et al., 2017). This suggests that the degree of dispersability may vary in different social spider species with varying consequences for gene flow. ...
Article
Dispersal is inherent to all living organisms. Sit-and-wait predators such as social spiders, with their sedentary lifestyles, present an intriguing and underexplored case to examine the proximate and ultimate reasons for dispersal. Though a reduction in dispersal tendencies must accompany the evolution of sociality in spiders, a fraction of the colony may disperse in groups or individually in many species. Such group or solitary dispersal by female social spiders in specific life stages, can lead to colony fission or colony foundation. Males move between colonies, however, there are no direct estimations of male dispersal distances for any species. The structured populations and high inbreeding within colonies suggest that dispersal events occur over limited spatial scales and may be mediated by extrinsic and intrinsic factors. Future studies exploring complex relationships between environmental variables, phenotypes of individuals, colony state and dispersal are advocated. Another area of interest is probing the dispersal process itself to understand the mechanisms of information transfer between individuals at the onset of dispersal. This involves designing studies to examine how break-away groups reach a consensus on when to disperse and where to go.
... For the reads that did not overlap, we reverse complemented the R2 sequence and trimmed the beginning (13 bp) and the end (6 bp) after visual exploration of sequence quality in FastQC. We then concatenated the two paired-end reads using a Python script adapted from Settepani et al. (2017). At the end, both merged and concatenated reads (174 bp) were pooled together into individual FASTQ files. ...
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Sandeels are an ecologically important group of fishes; they are a key part of the food chain serving as food for marine mammals, seabirds and fish. Sandeels are further targeted by a large industrial fishery, which has led to concern about ecosystem effects. In the North Sea, the lesser sandeel Ammodytes marinus is by far the most prevalent species of sandeel in the fishery. Management of sandeel in the North Sea plus the Kattegat is currently divided into seven geographical areas, based on subtle differences in demography, population dynamics and results from simulations of larval dispersal. However, little is known about the underlying genetic population structure. In this study, we used 2522 SNPs derived from Restriction‐site Associated DNA sequencing (RADseq) typed in 429 fish representing four main sandeel management areas. Our main results showed i) a lack of a clear spatially defined genetic structure across the majority of genetic markers, and ii) the existence of a group of at least 13 SNPs under strong linkage disequilibrium which together separate North Sea sandeel into three haplotype clusters, suggestive of one or more structural variants in the genome. Analyses of the spatial distribution of these putative structural variants suggest at least partial reproductive isolation of sandeel in the western management area along the Scottish coast, supporting a separate management. Our results highlight the importance of the application of a large number of markers to be able to detect weak patterns of differentiation. This study contributes to increasing the genetic knowledge of this important exploited species, and results can be used to improve our understanding of population dynamics and stock structure.
... Females provision the offspring with regurgitated fluids and are consumed by their offspring about 2 weeks after hatching (Schneider, 1995). The social spider S. dumicola lives in communal nests, which arise from a single mated female and her offspring Settepani et al., 2017). Females oviposit December-February, and mothers and allomothers care cooperatively for the offspring for several months until they are consumed by the offspring (Seibt and Wickler, 1987;Salomon and Lubin, 2007). ...
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Some semelparous species show terminal investment by suicidal offspring provisioning. This requires internal cellular disintegration for the production of regurgitated food and in preparation for the sacrifice of the female body to the offspring, however, we have limited insights into the extent and costs of such physiological modifications. Extreme provisioning is hypothesized to be limited to reproducing individuals because it requires physiological alterations triggered by reproduction. However, non-reproducing helpers-at-the-nest have been shown to engage in suicidal provisioning, prompting us to ask whether helpers undergo similar physiological alterations to brood provisioning as mothers, which would represent an adaptation to cooperative breeding. Using an experimental approach, we investigated the physiological consequences of extended maternal care in the solitary spider Stegodyphus lineatus and the cooperative breeder S. dumicola, and whether non-reproducing helpers (virgin allomothers) in S. dumicola show physiological adaptations to brood provisioning. To identify costs of offspring provisioning, we determined the energy expenditure (standard metabolic rate; SMR) and tissue disintegration over the course of brood care. In both species, brood care is associated with elevated SMR, which was highest in allomothers. Brood care results in progressive disintegration of midgut tissue, which also occurred in allomothers. On experimental offspring removal, these responses are reversible but only until the onset of regurgitation feeding, marking a physiological “point-of-no-return.” The mechanism underlying the onset of physiological responses is unknown, but based on our finding of mature eggs in mothers and allomothers, as opposed to the undeveloped eggs in virgins of the solitary species, we propose that oocyte maturation is a central adaptation in non-reproducing helpers to provide terminal allomaternal care.
... A few studies provide similar estimates of Ne and t g for chelicerates. For example, Settepani et al. (2017) reports Ne = 594×10 3 for the social spider Stegodyphus mimosarum and Lynch (2005) reports Ne = 10 6 for invertebrates, while generation times range from a few days in some mites (7.5 days for T. urticae, Shih et al., 1976) to several years (13-14 for Limulus polyphemus, Sweka et al., 2007). Evidently, the simulation imposed biologically unrealistic assumptions such as panmixia and constant population sizes across taxa and the evolutionary time scale. ...
Article
Horseshoe crabs (Xiphosura) are traditionally regarded as sister group to the clade of terrestrial chelicerates (Arachnida). This hypothesis has been challenged by recent phylogenomic analyses, but the non-monophyly of Arachnida has consistently been disregarded as artifactual. We reevaluated the placement of Xiphosura among chelicerates using the most complete phylogenetic dataset to date, expanding outgroup sampling and including data from whole genome sequencing projects. In spite of uncertainty in the placement of some arachnid clades, all analyses show Xiphosura consistently nested within Arachnida as the sister group to Ricinulei (hooded tick spiders). It is apparent that the radiation of Arachnids is an old one and occurred over a brief period of time, resulting in several consecutive short internodes, and thus is a potential case for the confounding effects of incomplete lineage sorting (ILS). We simulated coalescent gene trees to explore the effects of increasing levels of ILS on the placement of horseshoe crabs. In addition, common sources of systematic error were evaluated, as well as the effects of fast evolving partitions and the dynamics of problematic long branch orders. Our results indicated that the placement of horseshoe crabs cannot be explained by missing data, compositional biases, saturation, or incomplete lineage sorting. Interrogation of the phylogenetic signal showed that the majority of loci favor the derived placement of Xiphosura over a monophyletic Arachnida. Our analyses support the inference that horseshoe crabs represent a group of aquatic arachnids, comparable to aquatic mites, breaking a long-standing paradigm in chelicerate evolution and altering previous interpretations of the ancestral transition to the terrestrial habitat. Future studies testing chelicerate relationships should approach the task with a sampling strategy where the monophyly of Arachnida is not held as the premise.
... In addition, eusociality within Synalpheus appears to be relatively stable, with only one estimated reversal to pair-living (Fig. 2) (Hultgren & Brandt 2015). The rarity and instability of eusociality observed in other taxa, and particularly in primitively eusocial species (Wilson & H€ olldobler 2005;Fu et al. 2014), can be attributed to its high extinction risk (Fu et al. 2014), which is driven primarily by reduced genetic diversity due to inbreeding (Agnarsson et al. 2006;Settepani et al. 2017). It is possible that eusociality is more common and more stable in snapping shrimps relative to the eusocial insects because of the intense competition that shrimps experience over host sponges. ...
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Evidence from insects and vertebrates suggests that cooperation may have enabled species to expand their niches, becoming ecological generalists and dominating the ecosystems in which they occur. Consistent with this idea, eusocial species of sponge-dwelling Synalpheus shrimps from Belize are ecological generalists with a broader host breadth and higher abundance than non-eusocial species. We evaluate whether sociality promotes ecological generalism (social conquest hypothesis) or whether ecological generalism facilitates the transition to sociality (social transition hypothesis) in 38 Synalpheus shrimp species. We find that sociality evolves primarily from host generalists, and almost exclusively so for transitions to eusociality. Additionally, sponge volume is more important for explaining social transitions towards communal breeding than to eusociality, suggesting that different ecological factors may influence the independent evolutionary origins of sociality in Synalpheus shrimps. Ultimately, our results are consistent with the social transition hypothesis and the idea that ecological generalism facilitates the transition to sociality.
Article
Understanding the role of genetic and non‐genetic variants in modulating phenotypes is central to our knowledge of adaptive responses to local conditions and environmental change, particularly in species with such low population genetic diversity that it is likely to limit their evolutionary potential. A first step towards uncovering the molecular mechanisms underlying population specific responses to the environment is to carry out environmental association studies. We associated climatic variation with genetic, epigenetic and microbiome variation in populations of a social spider with extremely low standing genetic diversity. We identified genetic variants that associate strongly with environmental variation, particularly with average temperature, a pattern consistent with local adaptation. Variation in DNA methylation in many genes was strongly correlated with a wide set of climate parameters, thereby revealing a different pattern of associations than that of genetic variants, which show strong correlations to a more restricted range of climate parameters. DNA methylation levels were largely independent of cis‐genetic variation and of overall genetic population structure, suggesting that DNA methylation can work as an independent mechanism. Microbiome composition also correlated with environmental variation, but most strong associations were with precipitation related climatic factors. Our results suggest a role for both genetic and non‐genetic mechanisms in shaping phenotypic responses to local environments.
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Genome-wide methods offer a powerful approach to detect signatures of drug selection. However, limited availability of suitable reference genomes and the difficulty of obtaining field populations with well-defined, distinct drug treatment histories mean there is little information on the signatures of selection in parasitic nematodes and on how best to detect them. This study addresses these knowledge gaps by using field populations of Haemonchus contortus with well-defined benzimidazole treatment histories, leveraging a recently completed chromosomal-scale reference genome assembly. We generated a panel of 49,393 genomic markers to genotype 20 individual adult worms from each of four H. contortus populations: two from closed sheep flocks with an approximate 20 year history of frequent benzimidazole treatment, and two populations with a history of little or no treatment. Sampling occurred in the same geographical region to limit genetic differentiation and maximize the detection sensitivity. A clear signature of selection was detected on chromosome I, centered on the isotype-1 β-tubulin gene. Two additional, but weaker, signatures of selection were detected; one near the middle of chromosome I spanning 3.75 Mbp and 259 annotated genes, and one on chromosome II spanning a region of 3.3 Mbp and 206 annotated genes, including the isotype-2 β-tubulin locus. We also assessed how sensitivity was impacted by sequencing depth, worm number, and pooled versus individual worm sequence data. This study provides the first known direct genome-wide evidence for any parasitic nematode, that the isotype-1 β-tubulin gene is quantitatively the single most important benzimidazole resistance locus. It also identified two additional genomic regions that likely contain benzimidazole resistance loci of secondary importance. This study provides an experimental framework to maximize the power of genome-wide approaches to detect signatures of selection driven by anthelmintic drug treatments in field populations of parasitic nematodes.
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Although eusocial animals often achieve ecological dominance in the ecosystems where they occur, many populations are unstable, resulting in local extinction. Both patterns may be linked to the characteristic demography of eusocial species—high reproductive skew and reproductive division of labor support stable effective population sizes that make eusocial groups more competitive in some species, but also lower effective population sizes that increase susceptibility to population collapse in others. Here, we examine the relationship between demography and social organization in Synalpheus snapping shrimps, a group in which eusociality has evolved recently and repeatedly. We show using coalescent demographic modelling that eusocial species have had lower but more stable effective population sizes across 100,000 generations. Our results are consistent with the idea that stable population sizes may enable competitive dominance in eusocial shrimps, but they also suggest that recent population declines are likely caused by eusocial shrimps’ heightened sensitivity to environmental changes, perhaps as a result of their low effective population sizes and localized dispersal. Thus, although the unique life histories and demography of eusocial shrimps have likely contributed to their persistence and ecological dominance over evolutionary timescales, these social traits may also make them vulnerable to contemporary environmental change.
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Genome-wide methods offer a powerful approach to detect signatures of drug selection in parasite populations in the field. However, their application to parasitic nematodes has been limited because of both a lack of suitable reference genomes and the difficulty of obtaining field populations with sufficiently well-defined drug selection histories. Consequently, there is little information on the genomic signatures of drug selection for parasitic nematodes in the field and on how best to detect them. This study was designed to address these knowledge gaps using field populations of Haemonchus contortus with well-defined and contrasting benzimidazole-selection histories, leveraging a recently completed chromosomal-scale reference genome assembly. We generated a panel of 49,393 ddRADseq markers and used this resource to genotype 20 individual H. contortus adult worms from each of four H. contortus populations: two from closed sheep flocks that had an approximately 20-year history of frequent treatment exclusively with benzimidazole drugs, and two populations with a history of little or no drug treatment. The populations were chosen from the same geographical region to limit population structure in order to maximize the sensitivity of the approach. A clear signature of selection was detected on the left arm of chromosome I centered on the isotype-1 β-tubulin gene in the benzimidazole-selected but not the unselected populations. Two additional, but weaker, signatures of selection were detected; one near the middle of chromosome I and one near the isotype-2 β-tubulin locus on chromosome II. We examined genetic differentiation between populations, and nucleotide diversity and linkage disequilibrium within populations to define these two additional regions as encompassing five genes and a single gene. We also compared the relative power of using pooled versus individual worm sequence data to detect genomic selection signatures and how sensitivity is impacted by sequencing depth, worm number, and population structure. In summary, this study used H. contortus field populations with well-defined drug selection histories to provide the first direct genome-wide evidence for any parasitic nematode that the isotype-1 β-tubulin gene is the quantitatively most important benzimidazole resistance locus. It also identified two additional genomic regions that likely contain benzimidazole-resistance loci of secondary importance. Finally, this study provides an experimental framework to maximize the power of genome-wide approaches to detect signatures of selection driven by anthelmintic drug treatments in field populations of parasitic nematodes. AUTHOR SUMMARY Benzimidazoles are important anthelmintic drugs for human and animal parasitic nematode control with ∼0.5 billion children at risk of infection treated annually worldwide. Drug resistance is common in livestock parasites and a growing concern in humans. Haemonchus contortus is the most important model parasite system used to study anthelmintic resistance and a significant livestock pathogen. It is also one of the few parasitic nematodes with a chromosomal-scale genome assembly. We have undertaken genome-wide scans using a dense RADseq marker panel on worms from natural field populations under differing levels of benzimidazole selection. We show that there is a single predominant genomic signature of selection in H. contortus associated with benzimidazole selection centred on the isotype-1 β-tubulin locus. We also identify two weaker signatures of selection indicative of secondary drug resistance loci. Additionally, we assess the minimum data requirements for parameters including worm number, sequence depth, marker density needed to detect the signatures of selection and compare individual to Poolseq analysis. This work is the first genome-wide study in a parasitic nematode to provide direct evidence of the isotype-1 β-tubulin locus being the single predominant benzimidazole resistance locus and provides an experimental framework for future population genomic studies on anthelmintic resistance.
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Social spiders of the species Stegodyphus dumicola live in communal nests with hundreds of individuals and are characterized by extremely low-species wide genetic diversity. The lack of genetic diversity in combination with group-living imposes a potential threat for infection by pathogens. We therefore proposed that specific microbial symbionts inhabiting the spider nests may provide antimicrobial defense. To compare the bacterial and fungal diversity in 17 nests from three different locations in Namibia spider nests, we used 16S rRNA gene and internal transcribed spacer (ITS2) sequencing. The nest microbiomes differed between geographically distinct spider populations and appeared largely determined by the local environment. Nevertheless, we identified a core microbiome consisting of four bacterial genera (Curtobacterium, Modestobacter, Sphingomonas, Massilia) and four fungal genera (Aureobasidium, Didymella, Alternaria, Ascochyta), which likely are selected from surrounding soil and plants by the nest environment. We did not find indications for a strain- or species-specific symbiosis in the nests. Isolation of bacteria and fungi from nest material retrieved a few bacterial strains with antimicrobial activity but a number of antimicrobial fungi, including members of the fungal core microbiome. The significance of antimicrobial taxa in the nest microbiome for host protection remains to be shown.
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Many animal societies are susceptible to mass mortality events and collapse. Elucidating how environmental pressures determine patterns of collapse is key for our understanding of social evolution. Using the social spider Stegodyphus dumicola we investigated the environmental drivers of colony extinction along two precipitation gradients across southern Africa, using the Namib and Kalahari deserts versus wetter savanna habitats to the north and east. We deployed experimental colonies (n = 242) along two 800km transects and returned to assess colony success in the field after two months. Specifically, we noted colony extinction events after the two-month duration and collected environmental data on the correlates of those extinction events (e.g., evidence of ant attacks, # prey captured). We found that colony extinction events at desert sites were more frequently associated with attacks by predatory ants as compared to savanna sites, while colony extinctions in wetter savannas sites were more tightly associated with fungal outbreaks. Our findings support the hypothesis that environments vary in the selection pressures that they impose on social organisms, which may explain why different social phenotypes are often favored in each habitat.
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Urbanization is a severe form of habitat fragmentation that can cause many species to be locally extirpated and many others to become trapped and isolated within an urban matrix. The role of drift in reducing genetic diversity and increasing genetic differentiation is well recognized in urban populations. However, explicit incorporation and analysis of the demographic and temporal factors promoting drift in urban environments is poorly studied. Here, we genotyped 15 microsatellites in 320 fire salamanders from the historical city of Oviedo (Est. 8(th) century) to assess the effects of time since isolation, demographic history (historical effective population size; Ne) and patch size on genetic diversity, population structure and contemporary Ne. Our results indicate that urban populations of fire salamanders are highly differentiated, most likely due to the recent Ne declines, as calculated in coalescence analyses, concomitant with the urban development of Oviedo. However, urbanization only caused a small loss of genetic diversity. Regression modelling showed that patch size was positively associated with contemporary Ne, while we found only moderate support for the effects of demographic history when excluding populations with unresolved history. This highlights the interplay between different factors in determining current genetic diversity and structure. Overall, the results of our study on urban populations of fire salamanders provides some of the very first insights into the mechanisms affecting changes in genetic diversity and population differentiation via drift in urban environments, a crucial subject in a world where increasing urbanization is forecasted. This article is protected by copyright. All rights reserved.
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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.
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Because mating systems affect population genetics and ecology, they are expected to impact the molecular evolution of species. Self-fertilizing species experience reduced effective population size, recombination rates and heterozygosity, which in turn should decrease the efficacy of natural selection, both adaptive and purifying, and the strength of meiotic drive processes such as GC-biased gene conversion. The empirical evidence is only partly congruent with these predictions, depending on the analyzed species, some, but not all, of the expected effects have been observed. One possible reason is that self-fertilization is an evolutionary dead-end, so that most current selfers recently evolved self-fertilization, and their genome has not yet been strongly impacted by selfing. Here we investigate the molecular evolution of two groups of freshwater snails in which mating systems have likely been stable for several millions of years. Analyzing coding sequence polymorphism, divergence and expression levels, we report a strongly reduced genetic diversity, decreased efficacy of purifying selection, slower rate of adaptive evolution and weakened codon usage bias/GC-biased gene conversion in the selfer Galba compared to the outcrosser Physa, in full agreement with theoretical expectations. Our results demonstrate that self-fertilization, when effective in the long run, is a major driver of population genomic and molecular evolutionary processes. Despite the genomic effects of selfing, Galba truncatula seems to escape the demographic consequences of the genetic load. We suggest that the particular ecology of the species may buffer the negative consequences of selfing, shedding new light on the dead-end hypothesis. © The Author 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
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Reproductive skew is the study of how reproduction is partitioned in animal societies. In many social animals reproduction is shared unequally and leads to a reproductive skew among group members. Skew theory investigates the genetic and ecological factors causal to the partitioning of reproduction in animal groups and may yield fundamental insights into the evolution of animal sociality. This book brings together new theory and empirical work, mostly in vertebrates, to test assumptions and predictions of skew models. It also gives an updated critical review of skew theory. The team of leading contributors cover a wide range of species, from insects to humans, and discuss both ultimate (evolutionary) and proximate (immediate) factors influencing reproductive skew. Academic researchers and graduate students alike with an interest in evolution and sociality will find this material stimulating and exciting.