Combined analyses of kinship and F_ST suggest potential drivers of chaotic genetic patchiness in high gene‐flow populations

Abstract

We combine kinship estimates with traditional F-statistics to explain contemporary drivers of population genetic differentiation despite high gene flow. We investigate range-wide population genetic structure of the California spiny (or red rock) lobster (Panulirus interruptus) and find slight, but significant global population differentiation in mtDNA (ΦST = 0.006, P = 0.001; Dest_Chao = 0.025) and seven nuclear microsatellites (FST = 0.004, P < 0.001; Dest_Chao = 0.03), despite the species’ 240- to 330-day pelagic larval duration. Significant population structure does not correlate with distance between sampling locations, and pairwise FST between adjacent sites often exceeds that among geographically distant locations. This result would typically be interpreted as unexplainable, chaotic genetic patchiness. However, kinship levels differ significantly among sites (pseudo-F16,988 = 1.39, P = 0.001), and ten of 17 sample sites have significantly greater numbers of kin than expected by chance (P < 0.05). Moreover, a higher proportion of kin within sites strongly correlates with greater genetic differentiation among sites (Dest_Chao, R2 = 0.66, P < 0.005). Sites with elevated mean kinship were geographically proximate to regions of high upwelling intensity (R2 = 0.41, P = 0.0009). These results indicate that P. interruptus does not maintain a single homogenous population, despite extreme dispersal potential. Instead, these lobsters appear to either have substantial localized recruitment or maintain planktonic larval cohesiveness whereby siblings more likely settle together than disperse across sites. More broadly, our results contribute to a growing number of studies showing that low FST and high family structure across populations can coexist, illuminating the foundations of cryptic genetic patterns and the nature of marine dispersal.

The application of genetics to marine management and conservation: examples from the Indo-Pacific

“…Most parentage studies have used fishes, although an expansion of using parentage and kinship relationships comes from a recent study on California spiny lobsters, Panulirus interruptus, which require 240-330 d of pelagic development prior to settlement. Despite high gene flow and extensive mixing, Iacchei et al (2013) showed specific populations, associated with upwelling fronts, contained significantly more kin than expected and were thus significantly differentiated from other sites throughout the species range.…”

Isolation by resistance across a complex coral reef seascape

“…This 'isolation by resistance' (IBR) pattern may be particularly evident when an organism's reproductive strategy involves a sedentary adult phase and a pelagic larval stage that is subject to prevailing currents. Complex ocean circulation can represent significant barriers to dispersal and can produce patterns of genetic structure that are often difficult to interpret; however, incorporating oceanographic mechanisms into the analyses of population genetic data has placed confounding patterns of genetic patchiness into more ecologically relevant contexts [18][19][20][21][22].…”

Candidate gene variation in gilthead sea bream reveals complex spatiotemporal selection patterns between marine and lagoon habitats

“…Hence, even if selection occurs during the planktonic stage (Johnson & Black 1984), genetic drift is thought to be the main force shaping genetic structuring among groups of settlers, sometimes promoting increased relatedness among individuals (e.g. Larson & Julian 1999, Planes & Lenfant 2002, Selkoe et al 2006, Iacchei et al 2013, Aglieri et al 2014, review in Hauser & Carvalho 2008. This phenomenon, called sweepstake recruitment, has been widely documented (Hellberg 2006, 2009, Selkoe et al 2008, Hedgecock & Pudovkin 2011.…”