ABSTRACT
How species thrive in a wide range of environments is a major focus of evolutionary biology. For many species, limited genetic diversity or gene flow among habitats means that phenotypic plasticity must play an important role in their capacity to tolerate environmental heterogeneity and to colonize new habitats. However, we have a limited understanding of the molecular components that govern plasticity in ecologically relevant phenotypes. We examined this hypothesis in a spider species (Stegodyphus dumicola) with extremely low species-wide genetic diversity that nevertheless occupies a broad range of thermal environments. We determined phenotypic responses to temperature stress in individuals from four climatic zones using common garden acclimation experiments to disentangle phenotypic plasticity from genetic adaptations. Simultaneously, we created data sets on multiple molecular modalities: the genome, the transcriptome, the methylome, the metabolome, and the bacterial microbiome to determine associations with phenotypic responses. Analyses of phenotypic and molecular associations reveal that acclimation responses in the transcriptome and metabolome correlate with patterns of phenotypic plasticity in temperature tolerance. Surprisingly, genes whose expression seemed to be involved in plasticity in temperature tolerance were generally highly methylated contradicting the idea that DNA methylation stabilizes gene expression. This suggests that the function of DNA methylation in invertebrates varies not only among species but also among genes. The bacterial microbiome was stable across the acclimation period; combined with our previous demonstrations that the microbiome is temporally stable in wild populations, this is convincing evidence that the microbiome does not facilitate plasticity in temperature tolerance. Our results suggest that population-specific variation in temperature tolerance among acclimation temperatures appears to result from the evolution of plasticity in mainly gene expression.
Subject(s)
DNA Methylation , Transcriptome , Animals , Acclimatization/genetics , Spiders/genetics , Spiders/physiology , Thermotolerance/genetics , Microbiota , Metabolome , Adaptation, Physiological/genetics , Phenotype , TemperatureABSTRACT
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 inland 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.
Subject(s)
Gryllidae , Acclimatization , Adaptation, Physiological/genetics , Altitude , Animals , Biological Evolution , Gryllidae/genetics , HumansABSTRACT
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.
ABSTRACT
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.
Subject(s)
Behavior, Animal , Body Size , Animals , Behavior, Animal/physiology , Biological Evolution , Correlation of Data , Phylogeny , Predatory Behavior , Social Behavior , SpidersABSTRACT
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.
Subject(s)
Biological Evolution , Spiders/genetics , X Chromosome/genetics , Animals , Genetic Variation , Male , Population Dynamics , Sex RatioABSTRACT
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.
ABSTRACT
Kin selected benefits of cooperation result in pronounced kin discrimination and nepotism in many social species and favour the evolution of sociality. However, low variability in relatedness among group members, infrequent competitive interactions with non-relatives, and direct benefits of cooperation may relax selection for nepotism. We tested this prediction in a permanently social spider, Stegodyphus dumicola that appears to fulfil these conditions. Sociality is a derived trait, and kin discrimination exists in sub-social closely related congeners and is likely a selective force in the sub-social route to permanent sociality in spiders. We examined whether social spiders show nepotism in cooperative feeding when genetic relatedness among group members was experimentally varied. We found no effect of relatedness on feeding efficiency, growth rate or participation in feeding events. Previous studies on sub-social species showed benefits of communal feeding with kin, indicating nepotistic cooperation. The lack of evidence for nepotism in the social species suggests that kin discrimination has been lost or is irrelevant in communal feeding. Our results are consistent with the hypothesis that the role of nepotism is diminished when cooperation evolves in certain genetic and ecological contexts, e.g. when intra-group genetic relatedness is homogeneous and encounters with competitors are rare.
Subject(s)
Behavior, Animal/physiology , Competitive Behavior/physiology , Cultural Evolution , Evolution, Molecular , Social Behavior , Spiders/genetics , Animals , Social Dominance , Spiders/physiologyABSTRACT
Like many other nocturnal arthropods, the amblypygid Phrynus pseudoparvulus is capable of homing. The environment through which these predators navigate is a dense and heterogeneous tropical forest understory and the mechanism(s) underlying their putatively complex navigational abilities are presently unknown. This study explores the sensory inputs that might facilitate nocturnal navigation in the amblypygid P. pseudoparvulus. Specifically, we use sensory system manipulations in conjunction with field displacements to examine the potential involvement of multimodal - olfactory and visual - stimuli in P. pseudoparvulus' homing behavior. In a first experiment, we deprived individuals of their olfactory capacity and displaced them to the opposite side of their home trees (<5m). We found that olfaction-intact individuals were more likely to be re-sighted in their home refuges than olfaction-deprived individuals. In a second experiment, we independently manipulated both olfactory and visual sensory capacities in conjunction with longer-distance displacements (8m) from home trees. We found that sensory-intact individuals tended to be re-sighted on their home tree more often than sensory-deprived individuals, with a stronger effect of olfactory deprivation than visual deprivation. Comparing across sensory modality manipulations, olfaction-manipulated individuals took longer to return to their home trees than vision-manipulated individuals. Together, our results indicate that olfaction is important in the nocturnal navigation of P. pseudoparvulus and suggest that vision may also play a more minor role.
Subject(s)
Arachnida/physiology , Homing Behavior/physiology , Olfactory Perception/physiology , Spatial Navigation/physiology , Visual Perception/physiology , Animals , Female , MaleABSTRACT
Spiders are ecologically important predators with complex venom and extraordinarily tough silk that enables capture of large prey. Here we present the assembled genome of the social velvet spider and a draft assembly of the tarantula genome that represent two major taxonomic groups of spiders. The spider genomes are large with short exons and long introns, reminiscent of mammalian genomes. Phylogenetic analyses place spiders and ticks as sister groups supporting polyphyly of the Acari. Complex sets of venom and silk genes/proteins are identified. We find that venom genes evolved by sequential duplication, and that the toxic effect of venom is most likely activated by proteases present in the venom. The set of silk genes reveals a highly dynamic gene evolution, new types of silk genes and proteins, and a novel use of aciniform silk. These insights create new opportunities for pharmacological applications of venom and biomaterial applications of silk.
Subject(s)
Genome/genetics , Insect Proteins/genetics , Silk/genetics , Spider Venoms/genetics , Spiders/genetics , Animals , Base Sequence , Evolution, Molecular , Peptide Hydrolases/genetics , Phylogeny , Sequence Analysis, DNAABSTRACT
Deciphering the mechanisms involved in shaping social structure is key to a deeper understanding of the evolutionary processes leading to sociality. Individual specialization within groups can increase colony efficiency and consequently productivity. Here, we test the hypothesis that within-group variation in individual personalities (i.e. boldness and aggression) can shape task differentiation. The social spider Stegodyphus sarasinorum (Eresidae) showed task differentiation (significant unequal participation) in simulated prey capture events across 10-day behavioural assays in the field, independent of developmental stage (level of maturation), eliminating age polyethism. Participation in prey capture was positively associated with level of boldness but not with aggression. Body size positively correlated with being the first spider to emerge from the colony as a response to prey capture but not with being the first to attack, and dispersal distance from experimental colonies correlated with attacking but not with emerging. This suggests that different behavioural responses to prey capture result from a complex set of individual characteristics. Boldness and aggression correlated positively, but neither was associated with body size, developmental stage or dispersal distance. Hence, we show that personalities shape task differentiation in a social spider independent of age and maturation. Our results suggest that personality measures obtained in solitary, standardized laboratory settings can be reliable predictors of behaviour in a social context in the field. Given the wealth of organisms that show consistent individual behavioural differences, animal personality could play a role in social organization in a diversity of animals.