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Combined analyses of kinship and FST 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 (?ST = 0.006, P = 0.001; D(est_Chao) = 0.025) and seven nuclear microsatellites (F(ST) = 0.004, P < 0.001; D(est_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-F(16,988) = 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 (D(est_Chao), R(2) = 0.66, P < 0.005). Sites with elevated mean kinship were geographically proximate to regions of high upwelling intensity (R(2) = 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 F(ST) and high family structure across populations can coexist, illuminating the foundations of cryptic genetic patterns and the nature of marine dispersal.

SUBMITTER: Iacchei M

PROVIDER: S-EPMC3749441 | biostudies-literature | 2013 Jul

REPOSITORIES: biostudies-literature

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Combined analyses of kinship and FST suggest potential drivers of chaotic genetic patchiness in high gene-flow populations.

Iacchei Matthew M Ben-Horin Tal T Selkoe Kimberly A KA Bird Christopher E CE García-Rodríguez Francisco J FJ Toonen Robert J RJ

Molecular ecology 20130701 13

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; D(est_Chao) = 0.025) and seven nuclear microsatellites (F(ST) = 0.004, P < 0.001; D(est_Chao) = 0.03), despite the specie ...[more]

PMID: 23802550

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Project description:BACKGROUND:Studies on marine community dynamics and population structures are limited by the lack of exhaustive knowledge on the larval dispersal component of connectivity. Genetic data represents a powerful tool in understanding such processes in the marine realm. When dealing with dispersion and connectivity in marine ecosystems, many evidences show patterns of genetic structure that cannot be explained by any clear geographic trend and may show temporal instability. This scenario is usually referred to as chaotic genetic patchiness, whose driving mechanisms are recognized to be selection, temporal shifts in local population dynamics, sweepstakes reproductive success and collective dispersal. In this study we focused on the marbled crab Pachygrapsus marmoratus that inhabits the rocky shores of the Mediterranean Sea, Black Sea and East Atlantic Ocean, and disperses through planktonic larvae for about 1 month. P. marmoratus exhibits unexpectedly low connectivity levels at local scale, although well-defined phylogeographic patterns across the species' distribution range were described. This has been explained as an effect of subtle geographic barriers or due to sweepstake reproductive success. In order to verify a chaotic genetic patchiness scenario, and to explore mechanisms underlying it, we planned our investigation within the Ligurian Sea, an isolated basin of the western Mediterranean Sea, and we genotyped 321 individuals at 11 microsatellite loci. RESULTS:We recorded genetic heterogeneity among our Ligurian Sea samples with the occurrence of genetic clusters not matching the original populations and a slight inter-population divergence, with the geographically most distant populations being the genetically most similar ones. Moreover, individuals from each site were assigned to all the genetic clusters. We also recorded evidences of self-recruitment and a higher than expected within-site kinship. CONCLUSIONS:Overall, our results suggest that the chaotic genetic patchiness we found in P. marmoratus Ligurian Sea populations is the result of a combination of differences in reproductive success, en masse larval dispersion and local larval retention. This study defines P. marmoratus as an example of marine spawner whose genetic pool is not homogenous at population level, but rather split in a chaotic mosaic of slightly differentiated genetic patches derived from complex and dynamic ecological processes.

Project description:Dispersal is one of the main determining factors of population structure. In the marine habitat, well-connected populations with large numbers of reproducing individuals are common but even so population structure can exist on a small-scale. Variation in dispersal patterns between populations or over time is often associated to geographic distance or changing oceanographic barriers. Consequently, detecting structure and variation in dispersal on a fine-scale within marine populations still remains a challenge. Here we propose and use a novel approach of combining a clustering model, early-life history trait information from fish otoliths, spatial coordinates and genetic markers to detect very fine-scale dispersal patterns. We collected 1573 individuals (946 adults and 627 juveniles) of the black-faced blenny across a small-scale (2 km) coastline as well as at a larger-scale area (<50 kms). A total of 178 single nucleotide polymorphism markers were used to evaluate relatedness patterns within this well-connected population. In our clustering models we categorized SHORT-range dispersers to be potential local recruits based on their high relatedness within and low relatedness towards other spatial clusters. Local retention and/or dispersal of this potential local recruitment varied across the 2 km coastline with higher frequency of SHORT-range dispersers towards the southwest of the area for adults. An inverse pattern was found for juveniles, showing an increase of SHORT-range dispersers towards the northeast. As we rule out selective movement and mortality from one year to the next, this pattern reveals a complex but not full genetic mixing, and variability in coastal circulation is most likely the main driver of this fine-scale chaotic genetic patchiness within this otherwise homogeneous population. When focusing on the patterns within one recruitment season, we found large differences in temperatures (from approx. 17 °C to 25 °C) as well as pelagic larval duration (PLD) for juveniles from the beginning of the season and the end of the season. We were able to detect fine-scale differences in LONG-range juvenile dispersers, representing distant migrants, depending on whether they were born at the beginning of the season with a longer PLD, or at the end of the reproductive season. The ability to detect such fine-scale dispersal patchiness will aid in our understanding of the underlying mechanisms of population structuring and chaotic patchiness in a wide range of species even with high potential dispersal abilities.

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Combined analyses of kinship and FST suggest potential drivers of chaotic genetic patchiness in high gene-flow populations.

Publications

Combined analyses of kinship and FST suggest potential drivers of chaotic genetic patchiness in high gene-flow populations.

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