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Demographic inference provides insights into the extirpation and ecological dominance of eusocial snapping shrimps

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Abstract

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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Although social behavior can have a strong genetic component, it can also result in selection on genome structure and function, thereby influencing the evolution of the genome itself. Here we explore the bidirectional links between social behavior and genome architecture by considering variation in social and/or mating behavior among populations (social polymorphisms) and across closely related species. We propose that social behavior can influence genome architecture via associated demographic changes due to social living. We establish guidelines to exploit emerging whole-genome sequences using analytical approaches that examine genome structure and function at different levels (regulatory vs structural variation) from the perspective of both molecular biology and population genetics in an ecological context.
Article
Cooperatively breeding animals occur in virtually every ecosystem on earth. Comparative and biogeographic studies suggest that both benign and harsh-as well as stable and fluctuating-environments can favor the evolution of cooperative breeding behavior. The fact that cooperative societies occur in environments of such contrasting quality creates a paradox of environmental quality and sociality. The dual benefits framework-which leads to the prediction that the ecological consequences of sociality (e.g., range size) vary depending on the benefits that individuals of each species receive by forming social groups-offers a potential resolution to this paradox. Here we use a case study of two avian lineages, starlings (Sturnidae) and hornbills (Bucerotidae), in which environmental unpredictability appears to have opposite effects on the evolution of cooperation to test the dual benefits framework. Consistent with previous work, harsh and unpredictable environments promote cooperative breeding behavior in starlings, which in turn leads to larger geographic ranges. However, cooperatively breeding hornbills occur in benign and stable environments, but sociality does not influence range size. Our study suggests that the paradox of environmental quality and sociality arises largely because cooperative breeding is an umbrella term encompassing social species that form groups for different reasons. We demonstrate that differentiating among the functional causes of social group formation is critical for developing a predictive framework for understanding the evolution of cooperative breeding behavior.
Article
Genome divergence is greatly influenced by gene flow during early stages of speciation. As populations differentiate, geographical barriers can constrain gene flow and so affect the dynamics of divergence and speciation. Current geography, specifically disjunction and continuity of ranges, is often used to predict the historical gene flow during the divergence process. We test this prediction in eight meliphagoid bird species complexes codistributed in four regions. These regions are separated by known biogeographic barriers across northern Australia and Papua New Guinea. We find that bird populations currently separated by terrestrial habitat barriers within Australia and marine barriers between Australia and Papua New Guinea have a range of divergence levels and probability of gene flow not associated with current range connectivity. Instead, geographic distance and historical range connectivity better predict divergence and probability of gene flow. In this dynamic environmental context, we also find support for a nonlinear decrease of the probability of gene flow during the divergence process. The probability of gene flow initially decreases gradually after a certain level of divergence is reached. Its decrease then accelerates until the probability is close to zero. This implies that although geographic connectivity may have more of an effect early in speciation, other factors associated with higher divergence may play a more important role in influencing gene flow midway through and later in speciation. Current geographic connectivity may then mislead inferences regarding potential for gene flow during speciation under a complex and dynamic history of geographic and reproductive isolation. This article is protected by copyright. All rights reserved.
Article
High‐throughput sequencing data have greatly improved our ability to understand the processes that contribute to current biodiversity patterns. The “vanishing refuge” diversification model is speculated for the coastal forests of eastern Africa, whereby some taxa have persisted and diversified between forest refugia, while others have switched to becoming generalists also present in non‐forest habitats. Complex arrangements of geographical barriers (hydrology and topography) and ecological gradients between forest and non‐forest habitats may have further influenced the region's biodiversity, but elucidation of general diversification processes has been limited by lack of suitable data. Here, we explicitly test alternative diversification modes in the coastal forests using genome‐wide single nucleotide polymorphisms, mtDNA, spatial and environmental data for three forest (Arthroleptis xenodactyloides, Leptopelis flavomaculatus and Afrixalus sylvaticus) and four generalist (Afrixalus fornasini, A. delicatus, Leptopelis concolor, L. argenteus) amphibians. Multiple analyses provide insight about divergence times, spatial population structure, dispersal barriers, environmental stability and demographic history. We reveal highly congruent intra‐specific diversity and population structure across taxa, with most divergences occurring during the late Pliocene and Pleistocene. Although stability models support the existence of some forest refugia, dispersal barriers and demographic models point toward idiosyncratic diversification modes across taxa. We identify a consistent role for riverine barriers in the diversification of generalist taxa, but mechanisms of diversification are more complex for forest taxa and potentially include topographical barriers, forest refugia and ecological gradients. Our work demonstrates the complexity of diversification processes in this region, which vary between forest and generalist taxa, but also for ecologically similar species with shared population boundaries. This article is protected by copyright. All rights reserved.
Article
Over the last four decades the Mexican Caribbean has experienced intensive coastal development, and change on the reef system condition has already been observed. This paper describes the reef system characteristics, at local and seascape scales, and discusses the current status and trends, considering the main research efforts from academia and Non-Governmental Organizations. To date, the coral cover of most reefs in the region is between 15 and 20%, following a slight recovery on mean coral cover over the last decade. During this same period, fleshy macroalgae and herbivorous fish biomass appear to have increased. At seascape scales, an increase of macroalgae and the loss of seagrass habitat have been observed. Considering that anthropogenic and environmental disturbances will most likely increase, the establishment of newly protected areas in the Mexican Caribbean is appropriate, but sufficient accompanying funding is required.
Chapter
Darwin famously described special difficulties in explaining social evolution in insects. More than a century later, the evolution of sociality - defined broadly as cooperative group living - remains one of the most intriguing problems in biology. Providing a unique perspective on the study of social evolution, this volume synthesizes the features of animal social life across the principle taxonomic groups in which sociality has evolved. The chapters explore sociality in a range of species, from ants to primates, highlighting key natural and life history data and providing a comparative view across animal societies. In establishing a single framework for a common, trait-based approach towards social synthesis, this volume will enable graduate students and investigators new to the field to systematically compare taxonomic groups and reinvigorate comparative approaches to studying animal social evolution.
Article
Coffee Leaf Rust, caused by Hemileia vastatrix (Hv), represents the biggest threat to coffee production worldwide and ranks amongst the most serious fungal diseases in history. Despite a recent series of outbreaks and emergence of hyper-virulent strains, the population evolutionary history and potential of this pathogen remains poorly understood. To address this issue, we used RADseq to generate ∼19,000 SNPs across a worldwide collection of 37 Hv samples. Contrarily to the longstanding idea that Hv represents a genetically unstructured and cosmopolitan species, our results reveal the existence of a cryptic species complex with marked host tropism. Using phylogenetic and pathological data, we show that one of these lineages (C3) infects almost exclusively the most economically valuable coffee species (tetraploids that include Coffea arabica and inter-specific hybrids) while the other lineages (C1-C2) are severely maladapted to these hosts but successfully infect diploid coffee species. Population dynamic analyses suggest that the C3 group may be a recent “domesticated” lineage that emerged via host-shift from diploid coffee hosts. We also found evidence of recombination occurring within this group, which could explain the high pace of pathotype emergence despite the low genetic variation. Moreover, genomic footprints of introgression between the C3 and C2 groups were discovered and raise the possibility that virulence factors may be quickly exchanged between groups with different pathogenic abilities. This work advances our understanding on the evolutionary strategies used by plant pathogens in agro-ecosystems with direct and far-reaching implications for disease control. This article is protected by copyright. All rights reserved.
Article
Penaeid shrimps are among the most economically important crustaceans, which provide an important global food source. These species exhibit complex body plans and novelties, such as segments and appendages, which render them interesting organisms for developmental biology study of crustaceans. However, limited genomic resources have been put forward for the researches of them. Here, we report the genome sequencing and draft assembly of two economically important penaeid shrimp species, Marsupenaeus japonicus and Penaeus monodon. A total of 132.86. Gb and 132.83. Gb sequencing data was obtained in the two shrimp species. The genome assembly, a total length of 1.94. Gb and 2.04. Gb in M. japonicus and P. monodon, respectively, covers more than 97% of coding regions. We further identified 626. Mb (34.96%) and 833. Mb (46.68%) repeats, 16,716 and 18,100 genes in these two genomes, respectively. We also identified Hox genes that are important to their body plans. These data will provide valuable resources for the study of selective breeding and some plastic biological characters of penaeid shrimps, including molting, lobstering, brooding eggs and sensitization in humans.
Article
Large genomic data sets generated with restriction site-associated DNA sequencing (RADseq), in combination with demographic inference methods, are improving our ability to gain insights into the population history of species. We used a simulation approach to examine the potential for RADseq data sets to accurately estimate effective population size (Ne) over the course of stable and declining population trends, and we compare the ability of two methods of analysis to accurately distinguish stable from steadily declining populations over a contemporary time scale (20 generations). Using a linkage disequilibrium-based analysis, individual sampling (i.e., n ≥ 30) had the greatest effect on Ne estimation and the detection of population size declines, with declines reliably detected across scenarios ~10 generations after they began. Coalescent-based inference required fewer sampled individuals (i.e., n = 15), and instead was most influenced by the size of the SNP data set, with 25,000–50,000 SNPs required for accurate detection of population trends and at least 20 generations after decline began. The number of samples available and targeted number of RADseq loci are important criteria when choosing between these methods. Neither method suffered any apparent bias due to the effects of allele dropout typical of RAD data. With an understanding of the limitations and biases of these approaches, researchers can make more informed decisions when designing their sampling and analyses. Overall, our results reveal that demographic inference using RADseq data can be successfully applied to infer recent population size change and may be an important tool for population monitoring and conservation biology.
Article
Spatial responses of species to past climate change depend on both intrinsic traits (climatic niche breadth, dispersal rates) and the scale of climatic fluctuations across the landscape. New capabilities in generating and analysing population genomic data, along with spatial modelling, have unleashed our capacity to infer how past climate changes have shaped populations, and by extension, complex communities. Combining these approaches, we uncover lineage diversity across four co-distributed lizards from the Australian Monsoonal Tropics and explore how varying climatic tolerances interact with regional climate history to generate common versus disparate responses to late Pleistocene change. We find more divergent spatial structuring and temporal demographic responses in the drier Kimberley region compared to the more mesic and consistently suitable Top End. We hypothesize that, in general, the effects of species’ traits on sensitivity to climate fluctuation will be more evident in climatically marginal regions. If true, this points to the need in climatically marginal areas to craft more species- (or trait-) specific strategies for persistence under future climate change. This article is protected by copyright. All rights reserved.
Article
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.
Article
We established replicated experimental populations of the annual plant Clarkia pulchella to evaluate the existence of a causal relationship between loss of genetic variation and population survival probability. Two treatments differing in the relatedness of the founders, and thus in the genetic effective population size (Ne ), were maintained as isolated populations in a natural environment. After three generations, the low Ne treatment had significantly lower germination and survival rates than did the high Ne treatment. These lower germination and survival rates led to decreased mean fitness in the low Ne populations: estimated mean fitness in the low Ne populations was only 21% of the estimated mean fitness in the high Ne populations. This inbreeding depression led to a reduction in population survival: at the conclusion of the experiment, 75% of the high Ne populations were still extant, whereas only 31% of the low Ne populations had survived. Decreased genetic effective population size, which leads to both inbreeding and the loss of alleles by genetic drift, increased the probability of population extinction over that expected from demographic and environmental stochasticity alone. This demonstrates that the genetic effective population size can strongly affect the probability of population persistence.
Article
Animal social organization varies from complex societies where reproduction is dominated by a single individual (eusociality) to those where reproduction is more evenly distributed among group members (communal breeding). Yet, how simple groups transition evolutionarily to more complex societies remains unclear. Competing hypotheses suggest that eusociality and communal breeding are alternative evolutionary endpoints, or that communal breeding is an intermediate stage in the transition towards eusociality. We tested these alternative hypotheses in sponge-dwelling shrimps, Synalpheus spp. Although species varied continuously in reproductive skew, they clustered into pair-forming, communal and eusocial categories based on several demographic traits. Evolutionary transition models suggested that eusocial and communal species are discrete evolutionary endpoints that evolved independently from pair-forming ancestors along alternative paths. This ‘family-centred’ origin of eusociality parallels observations in insects and vertebrates, reinforcing the role of kin selection in the evolution of eusociality and suggesting a general model of animal social evolution.
Article
Using data from 83 isolates from a single population, the population genomics of the microcrustacean Daphnia pulex are described and compared to current knowledge for the only other well-studied invertebrate, Drosophila melanogaster These two species are quite similar with respect to effective population sizes and mutation rates, although some features of recombination appear to be different, with linkage disequilibrium being elevated at short (< 100 bp) distances in D. melanogaster and at long distances in D. pulex The study population adheres closely to the expectations under Hardy-Weinberg equilibrium, and reflects a past population history of no more than a two-fold range of variation in effective population size. Four-fold redundant silent sites and a restricted region of intronic sites appear to evolve in a nearly neutral fashion, providing a powerful tool for population-genetic analyses. Amino-acid replacement sites are predominantly under strong purifying selection, as are a large fraction of sites in UTRs and intergenic regions, but the majority of SNPs at such sites that rise to frequencies > 0:05 appear to evolve in a nearly neutral fashion. All forms of genomic sites (including replacement sites within codons, and intergenic and UTR regions) appear to be experiencing an ~ 2x higher level of selection scaled to the power of drift in D. melanogaster, but this may in part be a consequence of recent demographic changes. These results establish D. pulex as an excellent system for future work on the evolutionary genomics of natural populations.
Article
Group living occurs in two different forms in spiders, cooperatively breeding social species and colonial species. The social species construct a communal nest and capture web, capture prey and feed together and cooperate in raising the young. Social spiders lack pre-mating dispersal, which results in regular inbreeding within colonies. Social species are thought to be derived from subsocial forms, which have lengthy maternal care and some cooperation among young, but pre-mating dispersal of juveniles limits inbreeding. There are currently only 25 known social species occurring in seven different families and representing perhaps 19 independent evolutionary transitions to sociality. Colonial group living is much more common and occurs in a wide range of forms, from short-lived or long-lived aggregations of web-building spiders to communal nesting of active hunting species. Colonial species generally do not cooperate in prey capture and feeding, though there are exceptions; they do not cooperate in brood care; they have pre-mating dispersal and are outbred. Coloniality is likely derived from aggregation at rich food sources or nesting sites. Cooperation in the colonial species takes the form of sharing silk structures such as frame threads and nesting sites. The benefits of close proximity include the capture of larger prey and reduced variance in prey amount per spider and early warning of the presence of predators or parasites. However, group living carries costs of greater visibility both to potential prey and to predators and parasites. These benefits and costs are similar in cooperative-breeding and colonial species, while the main differences between them lie in degree of cooperation and the mating and breeding systems.
Article
The genomes of contemporary humans contain considerable information about the history of our species. Although the general contours of human evolutionary history have been defined with increasing resolution throughout the past several decades, the continuing deluge of massively large sequencing data sets presents new opportunities and challenges for understanding human evolutionary history. Here, we review the signatures that demographic history imparts on patterns of DNA sequence variation, statistical methods that have been developed to leverage information contained in genome-scale data sets and insights gleaned from these studies. We also discuss the importance of using exploratory analyses to assess data quality, the strengths and limitations of commonly used population genomics methods, and factors that confound population genomics inferences.
Article
Inferring demographic history is an important task in population genetics. Many existing inference methods are based on predefined simplified population models, which are more suitable for hypothesis testing than exploratory analysis. We developed a novel model-flexible method called stairway plot, which infers changes in population size over time using SNP frequency spectra. This method is applicable for whole-genome sequences of hundreds of individuals. Using extensive simulation, we demonstrate the usefulness of the method for inferring demographic history, especially recent changes in population size. We apply the method to the whole-genome sequence data of 9 populations from the 1000 Genomes Project and show a pattern of fluctuations in human populations from 10,000 to 200,000 years ago.
Article
Understanding the evolutionary processes driving the adaptive differentiation of populations is of broad interest in biology. Genome-wide nucleotide polymorphisms provide the basis for population genetic studies powered by advances in high-throughput sequencing technologies. These advances have led to an extension of genome projects to a variety of non-genetic model organisms, broadening our view on the evolution of gene families and taxonomic-restricted novelties. Here, we review the progress of genome projects in non-Drosophila arthropods, focusing on advances in the analysis of large-scale polymorphism data and functional genomics and examples of population genomic studies. © The Author 2015. Published by Oxford University Press. All rights reserved. For permissions, please email: journals.permissions@oup.com.
Article
A wide range of studies in population genetics have employed the sample frequency spectrum (SFS), a summary statistic which describes the distribution of mutant alleles at a polymorphic site in a sample of DNA sequences. In particular, recently there has been growing interest in analyzing the joint SFS data from multiple populations to infer parameters of complex demographic histories, including variable population sizes, population split times, migration rates, admixture proportions, and so on. Although much methodological progress has been made, existing SFS-based inference methods suffer from numerical instability and high computational complexity when multiple populations are involved and the sample size is large. In this paper, we present new analytic formulas and algorithms that enable efficient computation of the expected joint SFS for multiple populations related by a complex demographic model with arbitrary population size histories (including piecewise exponential growth). Our results are implemented in a new software package called momi (MOran Models for Inference). Through an empirical study involving tens of populations, we demonstrate our improvements to numerical stability and computational complexity.
Article
Can success be usefully defined in ants, and if so, which if any evolutionary strategies consistently confer it?-from Author