Sweepstakes Reproductive Success in Highly Fecund Marine Fish and Shellfish: A Review and Commentary

Abstract

Most marine animal species are very abundant, relatively long-lived, and late-maturing, with highly fecund adults adapted to spatially and temporally fluctuating ocean environments. Adults typically produce millions of small eggs that develop rapidly, without parental care, into planktonic larval stages that suffer high early mortality (Type III survivorship). Yet, large marine populations generally have only fractions of the genetic diversity expected from their sheer abundance, and despite widely dispersing larvae and geographically weakly structured adult populations, often show chaotic genetic heterogeneity on small spatial scales. These paradoxical observations can be explained by the hypothesis of Sweepstakes Reproductive Success (SRS), which posits extremely large variance in individual reproductive success, owing to sweepstakes-like chances of matching reproductive activity with oceanographic conditions conducive to gamete maturation, fertilization, larval development, settlement, and recruitment to the adult spawning population. The primary genetic consequence of SRS is reduction of Ne/N, the ratio of effective to actual population numbers, to a value usually much smaller than 0.01. Published nearly 30 yrs ago, SRS has gained traction, with numerous papers verifying specific predictions of the hypothesis in a broad array of marine animal taxa. Moreover, the hypothesis and empirical data from marine systems have stimulated modifications of coalescence population genetics theory, which can now account for low molecular diversity and chaotic patchiness. Here, we review the empirical and theoretical support for SRS, concluding that it plays a major role in shaping marine biodiversity, comment on issues related to hypothesis testing and data interpretation, and clarify some misconceptions.