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

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.

Parental care shapes the evolution of molecular genetic variation

“…In humans, benevolent social activities, such as modern health care, are thought to have led to the accumulation of deleterious mutations within populations [4,5]. Moreover, the capacity for co-operative brood care in insect societies to maintain and/or buffer against extreme changes in effective population size is thought to be a key determinant of population stability [6–8]. Therefore, the extent to which genetic variation is affected by social behaviour has implications for the health of populations and their capacity to rapidly adapt to environmental perturbations.…”

Parental care shapes the evolution of molecular genetic variation

“…Population genetic theory predicts that genetic diversity will increase with Ne and mutation rate ( Charlesworth, 2009 ). Previous empirical work linking behavioral and life-history traits, such as reproductive strategy, fecundity, and body size with genetic diversity has suggested that these associations are ultimately mediated by changes in Ne ( Bharti et al, 2023 ; Chak et al, 2022 ; Romiguier et al, 2014 ; Settepani et al, 2017 ). However, our results cannot be explained by demography because populations were maintained at similar population sizes with no differences in fecundity ( Schrader, 2017 ) and no possibility of overlapping generations and/or changes in mating structure.…”