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

Abstract

AbstractEusocial animals often achieve ecological dominance in the ecosystems where they occur, a process that may be linked to their demography. That is, reproductive division of labor and high reproductive skew in eusocial species is predicted to result in more stable effective population sizes that may make groups more competitive, but also lower effective population sizes that may make groups more susceptible to inbreeding and extinction. We examined the relationship between demography and social organization in one of the few animal lineages where eusociality has evolved recently and repeatedly among close relatives, theSynalpheussnapping shrimps. Although eusocial species often dominate the reefs where they occur by outcompeting their non-eusocial relatives for access to sponge hosts, many eusocial species have recently become extirpated across the Caribbean. Coalescent-based historical demographic inference in 12 species found that across nearly 100,000 generations, eusocial species tended to have lower but more stable effective population sizes through time. Our results are consistent with the idea that stable population sizes may enable eusocial shrimps to be more competitively dominant, but they also suggest that recent population declines are likely caused by eusocial shrimps’ heightened sensitivity to anthropogenically-driven environmental changes as a result of their low effective population sizes and localized dispersal, rather than to natural cycles of inbreeding and extinction. Thus, although the unique life histories and demography of eusocial shrimps has likely contributed to their persistence and ecological dominance over evolutionary timescales, these social traits may also make them vulnerable to contemporary environmental change.