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.

Climate drives the geography of marine consumption by changing predator communities.

The global distribution of primary production and consumption by humans (fisheries) is well-documented, but we have no map linking the central ecological process of consumption within food webs to temperature and other ecological drivers. Using standardized assays that span 105° of latitude on four continents, we show that rates of bait consumption by generalist predators in shallow marine ecosystems are tightly linked to both temperature and the composition of consumer assemblages. Unexpectedly, rates of consumption peaked at midlatitudes (25 to 35°) in both Northern and Southern Hemispheres across both seagrass and unvegetated sediment habitats. This pattern contrasts with terrestrial systems, where biotic interactions reportedly weaken away from the equator, but it parallels an emerging pattern of a subtropical peak in marine biodiversity. The higher consumption at midlatitudes was closely related to the type of consumers present, which explained rates of consumption better than consumer density, biomass, species diversity, or habitat. Indeed, the apparent effect of temperature on consumption was mostly driven by temperature-associated turnover in consumer community composition. Our findings reinforce the key influence of climate warming on altered species composition and highlight its implications for the functioning of Earth's ecosystems.

Ecological generalism facilitates the evolution of sociality in snapping shrimps.

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.

Evolutionary transitions towards eusociality in snapping shrimps.

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.

Synalpheus pinkfloydi sp. nov., a new pistol shrimp from the tropical eastern Pacific (Decapoda: Alpheidae).

A new, conspicuously coloured species of the alpheid genus Synalpheus Spence Bate, 1888, is described based on material collected on the Pacific coast of Panama. Synalpheus pinkfloydi sp. nov. is closely related to the western Atlantic S. antillensis Coutière, 1909, the two taxa being transisthmian, cryptic sister species. Both species are characterised by the distal areas of their major and minor chelae coloured in an intense, almost glowing pink-red. The morphological differences between S. pinkfloydi sp. nov. and S. antillensis Coutière, 1909 are subtle, being limited to the slightly different proportions of the merus of both chelipeds, distodorsal armature of the major cheliped merus, relative length of the antennal scaphocerite, and body size. However, they are genetically different with a 10.2% sequence divergence in COI. Based on molecular clock estimates, these transisthmian taxa diverged around 6.8-7.8 mya, i.e. well before the final closure of the Isthmus of Panama 2.5-3 mya.

Phylogenetic relationships within the snapping shrimp genus Synalpheus (Decapoda: Alpheidae).

The snapping shrimp genus Synalpheus (Alpheidae) is one of the most speciose decapod genera, with over 160 described species worldwide. Most species live in symbiotic relationships with other marine organisms, such as sponges, corals and crinoids, and some sponge-dwelling species have a highly organized, social structure. The present study is the first worldwide molecular phylogenetic analysis of Synalpheus, based on >2,200 bp of sequence data from two mitochondrial (COI and 16S) and two nuclear (PEPCK and 18S) loci. Our molecular data show strong support for monophyly of three out of six traditionally recognized morphology-based species groups: the S. brevicarpus, S. comatularum and S. gambarelloides groups. The remaining three species groups (S. paulsoni, S. neomeris and S. coutierei groups) are non-monophyletic in their current composition and will need to be either abandoned or taxonomically redefined. We also identified potential cryptic species of Synalpheus in our dataset, using intraspecific and interspecific sequence variation in COI from the taxonomically well-studied S. gambarelloides group to establish a genetic divergence threshold. We then used both genetic divergence and tree-based criteria (reciprocal monophyly) to identify potential cryptic species in the remaining taxa of the genus. Our results suggest the presence of multiple cryptic lineages in Synalpheus, underlining the need for more integrative taxonomic studies-including morphological, ecological, molecular, and color pattern data-in this biologically interesting genus.

Ecology and evolution affect network structure in an intimate marine mutualism.

Elucidating patterns and causes of interaction among mutualistic species is a major focus of ecology, and recent meta-analyses of terrestrial networks show that network-level reciprocal specialization tends to be higher in intimate mutualisms than in nonintimate mutualisms. It is largely unknown, however, whether this pattern holds for and what factors affect specialization in marine mutualisms. Here we present the first analysis of network specialization ([Formula: see text]) for marine mutualistic networks. Specialization among eight Indo-Pacific networks of obligate mutualistic gobies and shrimps was indistinguishable from that among comparably intimate terrestrial mutualisms (ants-myrmecophytes) and higher than that among nonintimate ones (seed dispersers). Specialization was affected by variability in habitat use for both gobies and shrimps and by phylogenetic history for shrimps. Habitat use was phylogenetically conserved among shrimp, and thus effects of shrimp phylogeny on partner choice were mediated in part by habitat. By contrast, habitat use and pairing patterns in gobies were not related to phylogenetic history. This asymmetry appears to result from evolutionary constraints on partner use in shrimps and convergence among distantly related gobies to utilize burrows provided by multiple shrimp species. Results indicate that the evolution of mutualism is affected by life-history characteristics that transcend environments and that different factors constrain interactions in disparate ecosystems.

Decline and local extinction of Caribbean eusocial shrimp.

The tropical shrimp genus Synalpheus includes the only eusocial marine animals. In much of the Caribbean, eusocial species have dominated the diverse fauna of sponge-dwelling shrimp in coral rubble for at least the past two decades. Here we document a recent, dramatic decline and apparent local extinction of eusocial shrimp species on the Belize Barrier Reef. Our collections from shallow reefs in central Belize in 2012 failed to locate three of the four eusocial species formerly abundant in the area, and showed steep declines in colony size and increases in frequency of queenless colonies prior to their disappearance. Concordant with these declines, several nonsocial, pair-forming Synalpheus species increased in frequency. The decline in eusocial shrimp is explained in part by disappearance of two sponge species on which they specialize. Eusocial shrimp collections from Jamaica in 2012 showed similar patterns of decline in colony size and increased queenlessness compared with prior Jamaican collections. The decline and local extinction of eusocial shrimp happened against a backdrop of changes in coral assemblages during recent decades, and may reflect changes in abundance and quality of dead coral substratum and succession of the diverse cryptic organisms living within it. These changes document potentially worrisome declines in a unique taxon of eusocial marine animals.

Phylogenetic community ecology and the role of social dominance in sponge-dwelling shrimp.

When functional traits are evolutionarily conserved, phylogenetic relatedness can serve as a proxy for ecological similarity to examine whether functional differences among species mediate community assembly. Using phylogenetic- and trait-based analyses, we demonstrate that sponge-dwelling shrimp (Synalpheus) assemblages are structured by size-based habitat filtering, interacting with competitive exclusion mediated by social system. Most shrimp communities were more closely related and/or more similar in size than randomized communities, consistent with habitat filtering facilitated by phylogenetically conserved body size. Those sponges with greater space heterogeneity hosted shrimp communities with greater size diversity, corroborating the importance of size in niche use. However, communities containing eusocial shrimp - which cooperatively defend territories - were less phylogenetically related and less similar in size, suggesting that eusociality enhances competitive ability and drives competitive exclusion. Our analyses demonstrate that community assembly in this diverse system occurs via traits mediating niche use and differential competitive ability.

Alternative camouflage strategies mediate predation risk among closely related co-occurring kelp crabs.

Although camouflage is a common predator defense strategy across a wide variety of organisms, direct tests of the adaptive and ecological consequences of camouflage are rare. In this study, we demonstrated that closely related crabs in the family Epialtidae coexist in the same algal environment but use alternative forms of camouflage--decoration and color change--to protect themselves from predation. Decoration and color change are both plastic camouflage strategies in that they can be changed to match different habitats: decoration occurs on a short timescale (hours to days), while color change accompanies molting and occurs on longer timescales (months). We found that the species that decorated the most had the lowest magnitude of color change (Pugettia richii); the species that decorated the least showed the highest magnitude of color change (Pugettia producta), and a third species (Mimulus foliatus) was intermediate in both decoration and color change, suggesting a negative correlation in utilization of these strategies. This negative correlation between color change and decoration camouflage utilization mirrored the effectiveness of these camouflage strategies in reducing predation in different species. Color camouflage primarily reduced predation on P. producta, while decoration camouflage (but not color camouflage) reduced predation on P. richii. These results indicate there might be among-species trade-offs in utilization and/or effectiveness of these two forms of plastic camouflage, with important consequences for distribution of these species among habitats and the evolution of different camouflage strategies in this group.

Predator diversity strengthens trophic cascades in kelp forests by modifying herbivore behaviour.

Although human-mediated extinctions disproportionately affect higher trophic levels, the ecosystem consequences of declining diversity are best known for plants and herbivores. We combined field surveys and experimental manipulations to examine the consequences of changing predator diversity for trophic cascades in kelp forests. In field surveys we found that predator diversity was negatively correlated with herbivore abundance and positively correlated with kelp abundance. To assess whether this relationship was causal, we manipulated predator richness in kelp mesocosms, and found that decreasing predator richness increased herbivore grazing, leading to a decrease in the biomass of the giant kelp Macrocystis. The presence of different predators caused different herbivores to alter their behaviour by reducing grazing, such that total grazing was lowest at highest predator diversity. Our results suggest that declining predator diversity can have cascading effects on community structure by reducing the abundance of key habitat-providing species.

The impacts of climate change in coastal marine systems.

Anthropogenically induced global climate change has profound implications for marine ecosystems and the economic and social systems that depend upon them. The relationship between temperature and individual performance is reasonably well understood, and much climate-related research has focused on potential shifts in distribution and abundance driven directly by temperature. However, recent work has revealed that both abiotic changes and biological responses in the ocean will be substantially more complex. For example, changes in ocean chemistry may be more important than changes in temperature for the performance and survival of many organisms. Ocean circulation, which drives larval transport, will also change, with important consequences for population dynamics. Furthermore, climatic impacts on one or a few 'leverage species' may result in sweeping community-level changes. Finally, synergistic effects between climate and other anthropogenic variables, particularly fishing pressure, will likely exacerbate climate-induced changes. Efforts to manage and conserve living marine systems in the face of climate change will require improvements to the existing predictive framework. Key directions for future research include identifying key demographic transitions that influence population dynamics, predicting changes in the community-level impacts of ecologically dominant species, incorporating populations' ability to evolve (adapt), and understanding the scales over which climate will change and living systems will respond.