The Recruitment Sweepstakes Has Many Winners: Genetic Evidence From the Sea Urchin Strongylocentrotus Purpuratus

Abstract

As a consequence of free spawning in the unpredictable nearshore environment, marine species with large fecundities and high pre-reproductive mortality may be subject to extreme variance in reproductive success. If the unpredictability of the ocean results in only a small subset of the adult population contributing to each larval cohort, then reproduction may be viewed as a sweepstakes, with chance events determining which adults are successful each spawning season. Such a reproductive sweepstakes scenario may partially account for large reductions in effective population sizes relative to census population sizes in marine species. We evaluated two predictions of the sweepstakes reproductive success hypothesis by testing: (1) whether sea urchin recruits contain reduced genetic variation relative to the adult population; and (2) whether cohorts of sea urchin recruits are genetically differentiated. Mitochondrial DNA sequences were collected from 283 recently settled Strongylocentrotus purpuratus recruits from four annual cohorts spanning seven years in locations throughout California. Observed haplotype numbers and haplotype diversities showed little evidence of reduced genetic variation in the recruits relative to the diversity estimated from a previously reported sample of 145 S. purpuratus adults. Different cohorts of recruits were in some cases mildly differentiated from each other. A computer simulation of sweepstakes recruitment indicates that our sampling strategy had sufficient statistical power to detect large variances in reproductive success.

Genetic patchiness in European eel adults evidenced by molecular genetics and population dynamics modelling

“…It has been hypothesized that life history traits of marine freespawning populations have partially evolved as a result of the unpredictability of spawning success (Flowers et al, 2002). In species with high pre-spawning mortalities, selection might favour allocation of more resources to growth/maintenance than reproduction, resulting in a longer life-span and a wider variance in maturity-at-age.…”

“…While the apparent absence of real barriers for fish/larvae displacement in marine environments could lead to a depression of the extent of genetic differentiation between subpopulations (Ward et al, 1994), several studies have detected significant heterogeneity among recruits on a small spatial scale in marine species dispersing via pelagic larvae, including gastropods (Johnson and Black, 1982), bivalves (Hedgecock, 1994;David et al, 1997;Li and Hedgecock, 1998), echinoderms (Edmands et al, 1996;Moberg and Burton, 2000;Flowers et al, 2002) and fish (Ruzzante et al, 1996;Planes and Lenfant, 2002;Pujolar et al, 2006Pujolar et al, , 2007. Hedgecock (1994) proposed that such genetic heterogeneity is likely to result from a large variance in reproductive success of parents.…”

Genetic patchiness among recruits in the European eel Anguilla anguilla

“…The observed homogeneity among winter samples contrasted with a marked differentiation among summer samples from the same locations, which was explained in part from changes in larval-source populations caused by seasonal changes in oceanographic conditions. Flowers et al (2002) argued that distinguishing between genetic patchiness due to gene flow among populations, or genetic drift within populations, is often impossible because the 2 processes occur simultaneously in most marine species' planktonic larval dispersal. The gene flow hypothesis implies the existence of different source populations, which contradicts field observations of a single reproductive area for European eel (Tesch 2003).…”

Temporal genetic homogeneity among shore crab (Carcinus maenas) larval events supplied to an estuarine system on the Portuguese northwest coast

“…In other surveys (Ruzzante et al, 1996;Moberg and Burton, 2000;Pujolar et al, 2006;, sweepstakes recruitment (Hedgecock, 1994) best explains the differentiation among cohorts but additional factors (for example, selection, spatial genetic variation, changes in larval delivery) could not be excluded. In contrast, some studies have found no reduced genetic diversity in recruits relative to estimates of diversity from adults (Flowers et al, 2002;Gilbert-Horvath et al, 2006;Rose et al, 2006;Calderó n et al, 2009), no measurable genetic differentiation of recruits over time (Gilbert-Horvath et al, 2006;Calderó n et al, 2009), no evidence of family structure (Hernbinger et al, 1997) and no reduction in effective population size (Poulsen et al, 2006) indicating little variance in reproductive success. It is evident therefore, that despite the prominence of stochastic larval supply events in the life histories of many marine animals no general trends can be derived from empirical observations.…”