Population Genetics of an Ecosystem-Defining Reef Coral Pocillopora damicornis in the Tropical Eastern Pacific

Abstract

BackgroundCoral reefs in the Tropical Eastern Pacific (TEP) are amongst the most peripheral and geographically isolated in the world. This isolation has shaped the biology of TEP organisms and lead to the formation of numerous endemic species. For example, the coral Pocillopora damicornis is a minor reef-builder elsewhere in the Indo-West Pacific, but is the dominant reef-building coral in the TEP, where it forms large, mono-specific stands, covering many hectares of reef. Moreover, TEP P. damicornis reproduces by broadcast spawning, while it broods mostly parthenogenetic larvae throughout the rest of the Indo-West Pacific. Population genetic surveys for P. damicornis from across its Indo-Pacific range indicate that gene flow (i.e. larval dispersal) is generally limited over hundreds of kilometers or less. Little is known about the population genetic structure and the dispersal potential of P. damicornis in the TEP.MethodologyUsing multilocus microsatellite data, we analyzed the population structure of TEP P. damicornis among and within nine reefs and test for significant genetic structure across three geographically and ecologically distinct regions in Panama.Principal Findings/ConclusionsWe detected significant levels of population genetic structure (global RST = 0.162), indicating restricted gene flow (i.e. larvae dispersal), both among the three regions (RRT = 0.081) as well as within regions (RSR = 0.089). Limited gene flow across a distinct environmental cline, like the regional upwelling gradient in Panama, indicates a significant potential for differential adaptation and population differentiation. Individual reefs were characterized by unexpectedly high genet diversity (avg. 94%), relatively high inbreeding coefficients (global FIS = 0.183), and localized spatial genetic structure among individuals (i.e. unique genets) over 10 m intervals. These findings suggest that gene flow is limited in TEP P. damicornis populations, particularly among regions, but even over meter scales within populations.

The importance of sampling design: spatial patterns and clonality in estimating the genetic diversity of coral reefs

“…For terrestrial plants, patterns of SGS arise largely due to their sedentary nature and dispersal-limited gametes (Vekemans and Hardy 2004). Reports of SGS for benthic marine organisms, however, are less common (but see Alberto et al 2005;Underwood et al 2007;Billingham et al 2007;Calderón et al 2007;Miller and Ayre 2008;Blanquer et al 2009;Ledoux et al 2010;Combosch and Vollmer 2011;Gorospe and Karl 2013). The fact that many benthic marine species have long-distance dispersal mechanisms may preclude them from small-scale patterns of genetic diversity (however, see Weersing andToonen 2009 andRiginos et al 2011) and the intense sampling effort required to detect SGS are both likely explanations for why SGS has only rarely been reported in marine systems.…”

“…Combosch and Vollmer (2011) working with P. damicornis in the tropical eastern Pacific (TEP) Ocean also found SGS within reefs. Their estimated Sp values, however, were considerably larger (0.049-0.062).…”

“…Furthermore, failure to incorporate spatial patterns when attempting to either characterize population structure or detect loci under selection can lead to high rates of type I error (i.e., false positives: incorrectly inferring population structure or signals of selection when there is none; Meirmans 2012). Yet while standard in population genetic studies of terrestrial plants (Heywood 1991), spatial autocorrelation analyses have only recently been employed in the study of genetic diversity in marine ecosystems (e.g., Alberto et al 2005;Billingham et al 2007;Calderón et al 2007;Underwood et al 2007;Miller and Ayre 2008;Blanquer et al 2009;Ledoux et al 2010;Combosch and Vollmer 2011;Pruner et al 2013;Gorospe and Karl 2013).…”

Marginal coral populations: the densest known aggregation of Pocillopora in the Galápagos Archipelago is of asexual origin

“…Here, we extend previous efforts (Combosch and Vollmer, 2011;Pinzón and Lajeunesse, 2011;Cunning et al, 2013;Pinzón et al, 2013) to evaluate the genetic diversity and population structure of Pocillopora in the Eastern Pacific at the geographic margins of this genus' range. By applying multilocus genotyping methods we discovered that the high density stand of Pocillopora corals at Isabela Islands was monogenotypic and aimed to determine whether this clone was a recent colonizer or a survivor of the large-scale ENSO events in 1982/83 and 1997/98.…”

“…Only three evolutionary divergent lineages were found based on mitochondrial sequencing phylogenies and Bayesian clustering analysis (Flot et al, 2008;Pinzón and Lajeunesse, 2011). The mismatch between genetic data and traditional species designations based on morphology calls into question previously published species distributions and occurrences of Pocillopora in the TEP and elsewhere (Combosch and Vollmer, 2011;Pinzón et al, 2013;Schmidt-Roach et al, 2013). A re-evaluation of Pocillopora species distribution in the TEP is thus necessary especially in light of recent large-scale disturbances during ENSO events that can cause local extirpations (Glynn and Deweerdt, 1991;Toth et al, 2012).…”