Reproductive Altruism, Social Diversity and Host Association in Sponge-Dwelling Snapping Shrimps, Synalpheus

The diversity of animal social strategies has interested evolutionary biologists since the time of Darwin. Eusociality—the apex of animal sociality—traditionally characterized by cooperative offspring care, overlapping generations and reproductive division of labor, was until recently known only in insects and a few vertebrate species. The independent evolution of eusociality in shrimps in the genus Synalpheus offers a unique opportunity to test the generality of social evolution theories that are based mainly on insects and social vertebrates. The genus Synalpheus is particularly ideal for comparative analysis because their social organizations are highly diverse, yet they share very similar ecology of being sponge dwellers. Further, their close associations with sponges, in which many are considered microbial fermenters, allow one to test the ecological drivers of species diversity in Synalpheus. In this dissertation, I first explored the nature and consequences of reproductive altruism in eusocial species. Chapter 1 showed that workers in eusocial Synalpheus retain reproductive capability, but reproduction of female workers is suppressed by the queen. Chapter 2 showed further that such reproductive inequity among females within a colony leads to potentially strong competition among females for reproductive opportunities, and is associated with reduced sexual dimorphism in eusocial Synalpheus species. Second, I examined the evolutionary trajectories between and ecological advantages associated with different social organizations in Synalpheus. Chapter 3 shows that the two demographically distinct social organizations found in Synalpheus—communality and eusociality—have evolved via separate evolutionary trajectories and represent alternative social strategies. Chapter 4 further shows that these social strategies are associated with different aspects of ecological advantages conferred on Synalpheus living together. Finally, the intimate association with host sponges constrains the lifestyle of Synalpheus and may be one factor that has predisposed their evolution of eusociality. In Chapter 5, I examined the association pattern of Synalpheus with their host sponges and found that the symbiotic microorganisms in sponges, rather than the phylogenetic histories of the host sponges, are a better predictor and potential driver of the host association pattern. This dissertation has sought to test, and ended up challenging, several paradigms in ecology and evolution. My results suggest that 1) polymorphic reproductive soldiers may represent a natural transition towards eusociality, 2) reproductive monopolization can modulate the pattern of sexual dimorphism in social species, 3) communality and eusociality evolved from distinct trajectories and have different ecological advantages, and 4) symbiotic microorganisms may mediate biological interactions between their hosts and other organisms

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

Dryad_TERAD_output_8spX4sample

Output from TERAD pipeline for 32 samples of Synalpheus snapping shrimps. The data has 8 species and 4 samples for each species. We compared TE composition between data from ddRADseq and LC-WGS in eight snapping shrimp species in the genus Synalpheus (Alpheidae). We used one sample per species for both ddRADseq and LC-WGS, and then added three additional samples (four total) per species for ddRADseq. For explanation of columns, see https://github.com/solomonchak/TERAD

Table A1. Sex and maturation status of adult workers.

Sex and maturation status of adult workers from five S. elizabethae colonies from the demosponge Lissodendoryx colombiensis collected from Bocas del Toro, Panama

Data from: Social control of reproduction and breeding monopolization in the eusocial snapping shrimp Synalpheus elizabethae

Understanding why individuals within altruistic societies forego 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 S. 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

Data from: Reproductive skew drives patterns of sexual dimorphism in sponge-dwelling snapping shrimps

Sexual dimorphism is typically a result of strong sexual selection on male traits used in male–male competition and subsequent female choice. However, in social species where reproduction is monopolized by one or a few individuals in a group, selection on secondary sexual characteristics may be strong in both sexes. Indeed, sexual dimorphism is reduced in many cooperatively breeding vertebrates and eusocial insects with totipotent workers, presumably because of increased selection on female traits. Here, we examined the relationship between sexual dimorphism and sociality in eight species of Synalpheus snapping shrimps that vary in social structure and degree of reproductive skew. In species where reproduction was shared more equitably, most members of both sexes were physiologically capable of breeding. However, in species where reproduction was monopolized by a single individual, a large proportion of females—but not males—were reproductively inactive, suggesting stronger reproductive suppression and conflict among females. Moreover, as skew increased across species, proportional size of the major chela—the primary antagonistic weapon in snapping shrimps—increased among females and sexual dimorphism in major chela size declined. Thus, as reproductive skew increases among Synalpheus, female–female competition over reproduction appears to increase, resulting in decreased sexual dimorphism in weapon size

Table A3. Gonadal development of workers with initial gonadal development

Gonadal development of the worker that had the most advanced development in each group under three experimental treatments where workers had initial gonadal developmen

Synalpheus dimorphism_all mature individuals

Sex, gonad maturity and size of each mature individua

Table A2. Gonadal development of workers

Gonadal development of the worker that had the most advanced development in each group under three experimental treatments. 1Q/6W: one queen and six workers; 0Q/6W: queenless with six workers (0Q/6W); and 0Q/1W: one worker only. Numbers in the table represent counts of groups. We have excluded 10, 10 and 4 groups from treatments 0Q/1W, 1Q/6W and 0Q/6W respectively, because either workers had initial gonadal development, the queen died, the group had only male workers, or the group had only female workers