Integrating larval connectivity with local demography reveals regional dynamics of a marine metapopulation.

Many ocean species exist within what are called marine metapopulations: networks of otherwise isolated local populations connected by the exchange of larval offspring. In order to manage these species as effectively as possible (e.g., by designing and implementing effective networks of marine protected areas), we must know how many offspring are produced within each local population (i.e., local demography), and where those offspring disperse (i.e., larval connectivity). Although there is much interest in estimating connectivity in the relatively simple sense of identifying the locations of spawning parents and their settling offspring, true measures of demographic connectivity that account for among-site variation in offspring production have been lacking. We combined detailed studies of local reproductive output and larval dispersal of a coral reef fish to quantify demographic connectivity within a regional metapopulation that included four widely spaced islands in the Bahamas. We present a new method for estimating demographic connectivity when the levels of dispersal among populations are inferred by the collection of genetically "tagged" offspring. We estimated that 13.3% of recruits returned to natal islands, on average (95% CI = 1.1-50.3%), that local retention was high on one of the islands (41%, 95% CI = 6.0-97.0%), and that larval connectivity was appreciable, even between islands 129 km apart (mean = 1.6%, 95% CI = 0.20-8.8%). Our results emphasize the importance of properly integrating measurements of production with measurements of connectivity. Had we not accounted for among-site variation in offspring production, our estimates of connectivity would have been inaccurate by a factor as much as 6.5. At a generational timescale, lifetime offspring production varied substantially (a fivefold difference among islands) and the importance of each island to long-term metapopulation growth was dictated by both larval production and connectivity. At the scale of our study (local populations inhabiting 5-ha reefs), the regional metapopulation could not grow without external input. However, an exploratory analysis simulating a network of four marine protected areas suggested that reserves of >65 ha each would ensure persistence of this network. Thus, integrating studies of larval connectivity and local demography hold promise for both managing and conserving marine metapopulations effectively.

Spatial and temporal patterns of larval dispersal in a coral-reef fish metapopulation: evidence of variable reproductive success.

Many marine organisms can be transported hundreds of kilometres during their pelagic larval stage, yet little is known about spatial and temporal patterns of larval dispersal. Although traditional population-genetic tools can be applied to infer movement of larvae on an evolutionary timescale, large effective population sizes and high rates of gene flow present serious challenges to documenting dispersal patterns over shorter, ecologically relevant, timescales. Here, we address these challenges by combining direct parentage analysis and indirect genetic analyses over a 4-year period to document spatial and temporal patterns of larval dispersal in a common coral-reef fish: the bicolour damselfish (Stegastes partitus). At four island locations surrounding Exuma Sound, Bahamas, including a long-established marine reserve, we collected 3278 individuals and genotyped them at 10 microsatellite loci. Using Bayesian parentage analysis, we identified eight parent-offspring pairs, thereby directly documenting dispersal distances ranging from 0 km (i.e., self-recruitment) to 129 km (i.e., larval connectivity). Despite documenting substantial dispersal and gene flow between islands, we observed more self-recruitment events than expected if the larvae were drawn from a common, well-mixed pool (i.e., a completely open population). Additionally, we detected both spatial and temporal variation in signatures of sweepstakes and Wahlund effects. The high variance in reproductive success (i.e., 'sweepstakes') we observed may be influenced by seasonal mesoscale gyres present in the Exuma Sound, which play a prominent role in shaping local oceanographic patterns. This study documents the complex nature of larval dispersal in a coral-reef fish, and highlights the importance of sampling multiple cohorts and coupling both direct and indirect genetic methods in order disentangle patterns of dispersal, gene flow and variable reproductive success.

Self-recruitment and sweepstakes reproduction amid extensive gene flow in a coral-reef fish.

Identifying patterns of larval dispersal within marine metapopulations is vital for effective fisheries management, appropriate marine reserve design, and conservation efforts. We employed genetic markers (microsatellites) to determine dispersal patterns in bicolour damselfish (Pomacentridae: Stegastes partitus). Tissue samples of 751 fish were collected in 2004 and 2005 from 11 sites encompassing the Exuma Sound, Bahamas. Bayesian parentage analysis identified two parent-offspring pairs, which is remarkable given the large population sizes and 28 day pelagic larval duration of bicolour damselfish. The two parent-offspring pairs directly documented self-recruitment at the two northern-most sites, one of which is a long-established marine reserve. Principal coordinates analyses of pair-wise relatedness values further indicated that self-recruitment was common in all sampled populations. Nevertheless, measures of genetic differentiation (F(ST)) and results from assignment methods suggested high levels of gene flow among populations. Comparisons of heterozygosity and relatedness among samples of adults and recruits indicated spatially and temporally independent sweepstakes events, whereby only a subset of adults successfully contribute to subsequent generations. These results indicate that self-recruitment and sweepstakes reproduction are the predominant, ecologically-relevant processes that shape patterns of larval dispersal in this system.