Reconciling patterns of inter‐ocean molecular variance from four classes of molecular markers in blue marlin (Makaira nigricans)

Abstract

Different classes of molecular markers occasionally yield discordant views of population structure within a species. Here, we examine the distribution of molecular variance from 14 polymorphic loci comprising four classes of molecular markers within approximately 400 blue marlin individuals (Makaira nigricans). Samples were collected from the Atlantic and Pacific Oceans over 5 years. Data from five hypervariable tetranucleotide microsatellite loci and restriction fragment length polymorphism (RFLP) analysis of whole molecule mitochondrial DNA (mtDNA) were reported and compared with previous analyses of allozyme and single-copy nuclear DNA (scnDNA) loci. Temporal variance in allele frequencies was nonsignificant in nearly all cases. Mitochondrial and microsatellite loci revealed striking phylogeographic partitioning among Atlantic and Pacific Ocean samples. A large cluster of alleles was present almost exclusively in Atlantic individuals at one microsatellite locus and for mtDNA, suggesting that, if gene flow occurs, it is likely to be unidirectional from Pacific to Atlantic oceans. Mitochondrial DNA inter-ocean divergence (FST) was almost four times greater than microsatellite or combined nuclear divergences including allozyme and scnDNA markers. Estimates of Neu varied by five orders of magnitude among marker classes. Using mathematical and computer simulation approaches, we show that substantially different distributions of FST are expected from marker classes that differ in mode of inheritance and rate of mutation, without influence of natural selection or sex-biased dispersal. Furthermore, divergent FST values can be reconciled by quantifying the balance between genetic drift, mutation and migration. These results illustrate the usefulness of a mitochondrial analysis of population history, and relative precision of nuclear estimates of gene flow based on a mean of several loci.

Allozyme variation in European lobster (Homarus gammarus) throughout its distribution range

“…The level of genetic differentiation, however, among the European lobster samples as estimated from six polymorphic allozyme loci, was relatively low. The overall F ST value of 0.016 is in agreement with findings for other marine species (e.g., Buonaccorsi et al 2001;Stamatis et al 2004). The various tests for population differentiation and F ST comparisons, and to some degree the UPGMA dendrogram of genetic distance (Nei 1972), suggest four main groups: northern Norway (bootstrap value = 71), Netherlands (bootstrap value = 54), Aegean (bootstrap value = 78), and the other samples in the Atlantic group.…”

Mito-nuclear discordance in the degree of population differentiation in a marine goby

“…This explanation has been invoked for the discordant patterns in population differentiation between nuclear and mitochondrial markers for marine organisms, such as the blue marlin Makaira nigricans (Buonaccorsi et al, 2001), Patagonian toothfish Dissostichus eleginoides (Appleyard et al, 2002;Shaw et al, 2004) and the olive sea snake Aipysurus laevis (Lukoschek et al, 2008). Simulations in EASYPOP v.1.7 (Balloux, 2001) with specific biological information about the sand goby showed no difference with the simulations of the study by Buonaccorsi et al (2001) (results not shown). Moreover, P. minutus is known to be one of the most abundant fish species across almost its full range (Pasquaud et al, 2004;Ehrenberg et al, 2005;Maes et al, 2005).…”

“…Marine fish have the potential to have high N e , and therefore recently separated large populations may appear genetically homogeneous even in the complete absence of contemporary gene flow (Hauser and Carvalho, 2008). Simulations in the study by Buonaccorsi et al (2001) showed that differences in the magnitude of estimated population subdivision from nuclear and mitochondrial markers could be accounted for entirely by differences in effective population sizes and polymorphisms on F ST estimates. The haploid and maternalonly inheritance of mtDNA has an effective population size of one-quarter that of nuclear DNA, making it more susceptible to effects of genetic drift (Shaw et al, 2004).…”

“…The haploid and maternalonly inheritance of mtDNA has an effective population size of one-quarter that of nuclear DNA, making it more susceptible to effects of genetic drift (Shaw et al, 2004). This explanation has been invoked for the discordant patterns in population differentiation between nuclear and mitochondrial markers for marine organisms, such as the blue marlin Makaira nigricans (Buonaccorsi et al, 2001), Patagonian toothfish Dissostichus eleginoides (Appleyard et al, 2002;Shaw et al, 2004) and the olive sea snake Aipysurus laevis (Lukoschek et al, 2008). Simulations in EASYPOP v.1.7 (Balloux, 2001) with specific biological information about the sand goby showed no difference with the simulations of the study by Buonaccorsi et al (2001) (results not shown).…”

“…Among those, mtDNA shows a higher sensitivity to resolve the phylogeographical and population genetic structure (Peijnenburg et al, 2006;Lukoschek et al, 2008). This discordance in resolution among markers may result from the differential effects of genetic drift, mutation and migration on a marker class, or may result from selection or sex-biased dispersal (Buonaccorsi et al, 2001). More research is required to study how common and important those factors are in the marine environment.…”