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

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 modeling 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 time scales, these social traits may also make them vulnerable to contemporary environmental change.

Correlated evolution of larval development, egg size and genome size across two genera of snapping shrimp.

Across plants and animals, genome size is often correlated with life-history traits: large genomes are correlated with larger seeds, slower development, larger body size and slower cell division. Among decapod crustaceans, caridean shrimps are among the most variable both in terms of genome size variation and life-history characteristics such as larval development mode and egg size, but the extent to which these traits are associated in a phylogenetic context is largely unknown. In this study, we examine correlations among egg size, larval development and genome size in two different genera of snapping shrimp, Alpheus and Synalpheus, using phylogenetically informed analyses. In both Alpheus and Synalpheus, egg size is strongly linked to larval development mode: species with abbreviated development had significantly larger eggs than species with extended larval development. We produced the first comprehensive dataset of genome size in Alpheus (n = 37 species) and demonstrated that genome size was strongly and positively correlated with egg size in both Alpheus and Synalpheus. Correlated trait evolution analyses showed that in Alpheus, changes in genome size were clearly dependent on egg size. In Synalpheus, evolutionary path analyses suggest that changes in development mode (from extended to abbreviated) drove increases in egg volume; larger eggs, in turn, resulted in larger genomes. These data suggest that variation in reproductive traits may underpin the high degree of variation in genome size seen in a wide variety of caridean shrimp groups more generally.

Eusociality in snapping shrimps is associated with larger genomes and an accumulation of transposable elements.

Despite progress uncovering the genomic underpinnings of sociality, much less is known about how social living affects the genome. In different insect lineages, for example, eusocial species show both positive and negative associations between genome size and structure, highlighting the dynamic nature of the genome. Here, we explore the relationship between sociality and genome architecture in Synalpheus snapping shrimps that exhibit multiple origins of eusociality and extreme interspecific variation in genome size. Our goal is to determine whether eusociality leads to an accumulation of repetitive elements and an increase in genome size, presumably due to reduced effective population sizes resulting from a reproductive division of labor, or whether an initial accumulation of repetitive elements leads to larger genomes and independently promotes the evolution of eusociality through adaptive evolution. Using phylogenetically informed analyses, we find that eusocial species have larger genomes with more transposable elements (TEs) and microsatellite repeats than noneusocial species. Interestingly, different TE subclasses contribute to the accumulation in different species. Phylogenetic path analysis testing alternative causal relationships between sociality and genome architecture is most consistent with the hypothesis that TEs modulate the relationship between sociality and genome architecture. Although eusociality appears to influence TE accumulation, ancestral state reconstruction suggests moderate TE abundances in ancestral species could have fueled the initial transitions to eusociality. Ultimately, we highlight a complex and dynamic relationship between genome and social evolution, demonstrating that sociality can influence the evolution of the genome, likely through changes in demography related to patterns of reproductive skew.

Comparative mitochondrial genomics of sponge-dwelling snapping shrimps in the genus Synalpheus: Exploring differences between eusocial and non-eusocial species and insights into phylogenetic relationships in caridean shrimps.

The genus Synalpheus is a cosmopolitan clade of marine shrimps found in most tropical regions. Species in this genus exhibit a range of social organizations, including pair-forming, communal breeding, and eusociality, the latter only known to have evolved within this genus in the marine realm. This study examines the complete mitochondrial genomes of seven species of Synalpheus and explores differences between eusocial and non-eusocial species considering that eusociality has been shown before to affect the strength of purifying selection in mitochondrial protein coding genes. The AT-rich mitochondrial genomes of Synalpheus range from 15,421 bp to 15,782 bp in length and comprise, invariably, 13 protein-coding genes (PCGs), two ribosomal RNA genes, and 22 transfer RNA genes. A 648 bp to 994 bp long intergenic space is assumed to be the D-loop. Mitochondrial gene synteny is identical among the studied shrimps. No major differences occur between eusocial and non-eusocial species in nucleotide composition and codon usage profiles of PCGs and in the secondary structure of tRNA genes. Maximum likelihood phylogenetic analysis of the complete concatenated PCG complement of 90 species supports the monophyly of the genus Synalpheus and its family Alpheidae. Moreover, the monophyletic status of the caridean families Alvinocaridae, Atyidae, Thoridae, Lysmatidae, Palaemonidae, and Pandalidae within caridean shrimps are fully or highly supported by the analysis. We therefore conclude that mitochondrial genomes contain sufficient phylogenetic information to resolve relationships at high taxonomic levels within the Caridea. Our analysis of mitochondrial genomes in the genus Synalpheus contributes to the understanding of the coevolution between genomic architecture and sociality in caridean shrimps and other marine organisms.

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

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

The complete mitochondrial genome of the eusocial sponge-dwelling snapping shrimp Synalpheus microneptunus.

In the marine realm, eusociality is only known to have evolved within a clade of sponge-dwelling snapping shrimps in the genus Synalpheus. Deciphering the genomic underpinnings of eusociality in these marine shrimps has been limited by the sparse genomic resources in this genus. Here, we report, for a eusocial shrimp Synalpheus microneptunus, a complete mitochondrial genome (22X coverage) assembled from short Illumina 150 bp paired-end reads. The 15,603 bp long mitochondrial genome of S. microneptunus is AT-rich and includes 13 protein-coding genes (PCGs), 2 ribosomal RNA genes, 22 transfer RNA genes and an 834 bp intergenic region assumed to be the D-loop. The gene order is identical to that reported for most caridean shrimps and corresponds to the presumed Pancrustacean ground pattern. All PCGs showed signs of purifying selection, with KA/KS <<1 across the whole PCGs and most sliding windows within PCGs. Maximum-likelihood and Bayesian inference phylogenetic analyses of 13 PCGs and 68 terminals supports the monophyly of the Caridea and the family Alpheidae. The complete mitochondrial genome of the eusocial shrimp Synalpheus microneptunus will contribute to a better understanding of the selective pressures and rates of molecular evolution in marine eusocial animals.

TERAD: Extraction of transposable element composition from RADseq data.

Transposable elements (TEs) - selfish DNA sequences that can move within the genome - comprise a large proportion of the genomes of many organisms. Although low-coverage whole-genome sequencing can be used to survey TE composition, it is noneconomical for species with large quantities of DNA. Here, we utilize restriction-site associated DNA sequencing (RADSeq) as an alternative method to survey TE composition. First, we demonstrate in silico that double digest restriction-site associated DNA sequencing (ddRADseq) markers contain the same TE compositions as whole genome assemblies across arthropods. Next, we show empirically using eight Synalpheus snapping shrimp species with large genomes that TE compositions from ddRADseq and low-coverage whole-genome sequencing are comparable within and across species. Finally, we develop a new bioinformatic pipeline, TERAD, to extract TE compositions from RADseq data. Our study expands the utility of RADseq to study the repeatome, making comparative studies of genome structure for species with large genomes more tractable and affordable.

Social Control of Reproduction and Breeding Monopolization in the Eusocial Snapping Shrimp Synalpheus elizabethae.

Understanding why individuals within altruistic societies forgo reproduction to raise others' offspring has fascinated scientists since Darwin. Although worker polymorphism is thought to have evolved only in sterile workers, worker subcastes appear to be common among social invertebrates and vertebrates. We asked whether sterility accompanies eusociality and morphological differentiation in snapping shrimps (Synalpheus)-the only known marine eusocial group. We show that workers in Synalpheus elizabethae are reproductively totipotent and that female-but not male-gonadal development and mating are mediated by the presence of a queen, apparently without physical aggression. In queenless experimental colonies, a single immature female worker typically became ovigerous, and no female workers matured in colonies with a resident queen. Thus, eusocial shrimp workers retain reproductive totipotency despite signs of morphological specialization. The failure of most female workers to mature is instead facultative and mediated by the presence of the queen, ensuring her reproductive monopoly.

Permanent Genetic Resources added to Molecular Ecology Resources Database 1 April 2010 - 31 May 2010.

This article documents the addition of 396 microsatellite marker loci to the Molecular Ecology Resources Database. Loci were developed for the following species: Anthocidaris crassispina, Aphis glycines, Argyrosomus regius, Astrocaryum sciophilum, Dasypus novemcinctus, Delomys sublineatus, Dermatemys mawii, Fundulus heteroclitus, Homalaspis plana, Jumellea rossii, Khaya senegalensis, Mugil cephalus, Neoceratitis cyanescens, Phalacrocorax aristotelis, Phytophthora infestans, Piper cordulatum, Pterocarpus indicus, Rana dalmatina, Rosa pulverulenta, Saxifraga oppositifolia, Scomber colias, Semecarpus kathalekanensis, Stichopus monotuberculatus, Striga hermonthica, Tarentola boettgeri and Thermophis baileyi. These loci were cross-tested on the following species: Aphis gossypii, Sooretamys angouya, Euryoryzomys russatus, Fundulus notatus, Fundulus olivaceus, Fundulus catenatus, Fundulus majalis, Jumellea fragrans, Jumellea triquetra Jumellea recta, Jumellea stenophylla, Liza richardsonii, Piper marginatum, Piper aequale, Piper darienensis, Piper dilatatum, Rana temporaria, Rana iberica, Rana pyrenaica, Semecarpus anacardium, Semecarpus auriculata, Semecarpus travancorica, Spondias acuminata, Holigarna grahamii, Holigarna beddomii, Mangifera indica, Anacardium occidentale, Tarentola delalandii, Tarentola caboverdianus and Thermophis zhaoermii.