The pelagic larvae of many marine organisms can potentially disperse across hundreds of kilometers, but whether oceanographic or behavioral mechanisms can constrain dispersal over periods sufficient for the evolution of genetic differentiation remains unclear. Here, we concurrently examine larval duration and genetic population differentiation in a cleaner goby, Elacatinus evelynae, a member of the most species-rich genus of Caribbean reef fishes. Despite evidence for extended pelagic duration (21 days), populations of E. evelynae show strong genetic differentiation: among color forms (1.36 to 3.04% divergent at mitochondrial cytochrome b) and among island populations within color forms (⌽ ST up to 70%). These results suggest that marine populations can remain demographically closed for thousands of generations despite extended larval duration, and that recognition cues such as color may promote speciation when geographic barriers are transient or weak.Many marine organisms have pelagic larvae that can potentially interconnect distant populations through dispersal on ocean currents. If these larvae disperse as passive propagules on advective current flow, they will be transported among both near and distant island populations (1). Species with such broadly dispersing larvae should be genetically homogeneous over large spatial scales, thus compromising their ability to adapt to local conditions (2). If, however, pelagic larvae are retained near their natal populations by behavioral (3) or physical oceanographic (4) mechanisms, then populations would have a greater opportunity for genetic differentiation and local adaptation. Should local retention persist over many generations, marine populations undivided by strong physical barriers might nonetheless form new species or at least differentiate to levels where different management or conservation strategies would be warranted for different populations.Studies in which fluorescent tags and environmental trace elements were used as markers in otoliths-calcareous structures in the inner ear of fishes-from newly recruited juvenile fishes indicate that as many as 60% of a juvenile cohort may recruit to their natal populations, despite larval durations of 3 to 7 weeks (5, 6). However, exchange rates averaging just a single larval individual per generation among populations can be sufficient to hinder genetic differentiation caused by drift or weak selection (7). In the absence of biogeographic barriers, genetic analyses to date have failed to reveal significant population differentiation for species with broad larval-dispersal potential (8-10), including one species (bluehead wrasse, Thalassoma bifasciatum) shown by trace-element studies to have high larval retention (6). Here, we test for genetic differentiation among island populations separated by hundreds of kilometers in a Caribbean reef fish with pelagic larvae.Elacatinus (ϭGobiosoma) evelynae, a reef-dwelling cleaner goby, is widely distributed throughout the Bahamas and Caribbean Sea (Fig. 1). It belongs to the ...
The movements of larvae between marine populations are difficult to follow directly and have been the subject of much controversy, especially in the Caribbean. The debate centres on the degree to which populations are demographically open, such that depleted populations can be replenished by recruitment from distant healthy populations, or demographically closed and thus in need of local management. Given the depressed state of many tropical reef populations, the understanding of these movements now bears critically on the number, placement, and size of marine reserves. Most genetic analyses assume that dispersal patterns have been stable for thousands of generations, thus they commonly reflect past colonization histories more than ongoing dispersal. Recently developed multilocus genotyping approaches, however, have the demonstrated ability to detect both migration and population isolation over far shorter timescales. Previously, we developed five microsatellite markers and demonstrated them to be both Mendelian and coral-specific. Using these markers and Bayesian analyses, we show here that populations of the imperiled reef-building coral, Acropora palmata, have experienced little or no recent genetic exchange between the western and the eastern Caribbean. Puerto Rico is identified as an area of mixing between the two subregions. As a consequence of this regional isolation, populations in the western and eastern Caribbean should have the potential to adapt to local conditions and will require population-specific management strategies.
Successful dispersal between populations leaves a genetic wake that can reveal historical and contemporary patterns of connectivity. Genetic studies of differentiation in the sea suggest the role of larval dispersal is often tempered by adult ecology, that changes in differentiation with geographic distance are limited by disequilibrium between drift and migration, and that phylogeographic breaks reflect shared barriers to movement in the present more than common historical divisions. Recurring complications include the presence of cryptic species, selection on markers, and a failure to account for differences in heterozygosity among markers and species. A better understanding of effective population sizes is needed. Studies that infer parentage or kinship and coalescent analyses employing more markers are both likely to spur progress, with analyses based on linkage disequilibrium potentially bridging results from these studies and reconciling patterns that vary at ecological and evolutionary timescales.
Species that build the physical structure of ecosystems often reproduce clonally, both in terrestrial (e.g., grasses, trees) and marine (e.g., corals, seagrasses) environments. The degree of clonality may vary over a species' range in accordance with the relative success of sexual and asexual recruitment. High genotypic (clonal) diversity of structural species may promote the species diversity and resilience of ecosystems in the face of environmental extremes. Conversely, low genotypic diversity may indicate an asexual strategy to maintain resources and genetic variation during population decline. Here, we use microsatellite markers to assess geographic variation in clonality in the coral Acropora palmata sampled from 26 reefs in eight regions spanning its tropical western Atlantic range (n = 751). Caribbean‐wide, the ratio (±sd) of genets (Ng) to sampled ramets (N) was 0.51 ± 0.28. Within reefs (30–70 m) and among reefs (10–100 km) within regions, clonal structure varied from being predominantly asexual (Ng/N approaching 0) to purely sexual (Ng/N = 1). However, two genetically isolated regions (western and eastern Caribbean) differed in clonal structure: genotypically depauperate populations (Ng/N = 0.43 ± 0.31) with lower densities (0.13 ± 0.08 colonies/m2) characterized the western region, while denser (0.30 ± 0.21 colonies/m2), genotypically rich stands (Ng/N = 0.64 ± 0.17) typified the eastern Caribbean. Genotypic richness (standardized to sample size; Ng/N) and genotypic diversity (Go/Ge) were negatively related to colony density within each province (r2 = 0.49–0.66, P < 0.001), indicating that dense stands have higher rates of asexual recruitment than less dense populations. Asexual recruitment was not correlated with large‐scale disturbance history or abundance of large colonies (potential fragment sources) but was negatively correlated with shelf area (r2 = 0.57, P < 0.01). We argue that sexual recruitment is more prevalent in the eastern range of A. palmata than the west, and that these geographic differences in the contribution of reproductive modes to population structure may be related to habitat characteristics. The two populations of the threatened A. palmata differ fundamentally in reproductive character and may respond differently to environmental change.
Long-lived corals, the foundation of modern reefs, often follow ecological gradients, so that populations or sister species segregate by habitat. Adaptive divergence maintains sympatric congeners after secondary contact or may even generate species by natural selection in the face of gene flow. Such ecological divergence, initially between alternative phenotypes within populations, may be aided by immigrant inviability, especially when a long period separates larval dispersal and the onset of reproduction, during which selection can sort lineages to match different habitats. Here, we evaluate the strength of one ecological factor (depth) to isolate populations by comparing the genes and morphologies of pairs of depth-segregated populations of the candelabrum coral Eunicea flexuosa across the Caribbean. Eunicea is endemic to the Caribbean and all sister species co-occur. Eunicea flexuosa is widespread both geographically and across reef habitats. Our genetic analysis revealed two depth-segregated lineages. Field survivorship data, combined with estimates of selection coefficients based on transplant experiments, suggest that selection is strong enough to segregate these two lineages. Genetic exchange between the Shallow and Deep lineages occurred either immediately after divergence or the two have diverged with gene flow. Migration occurs asymmetrically from the Shallow to Deep lineage. Limited recruitment to reproductive age, even under weak annual selection advantage, is sufficient to generate habitat segregation because of the cumulative prolonged prereproductive selection. Ecological factors associated with depth can act as filters generating strong barriers to gene flow, altering morphologies, and contributing to the potential for speciation in the sea.
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