A possible explanation for the population size discrepancy in tuna (genus Thunnus) estimated from mitochondrial DNA and microsatellite data
Graphical abstract
Highlights
► We report ten new cases of population size discrepancy in five tuna species. ► Homoplasy of microsatellite alleles is not responsible for the discrepancy. ► The discrepancy may reflect behavioral differences between the sexes.
Introduction
Bos et al. (2008) recently published a molecular study of the historical demography of a population of eastern tiger salamanders (Ambystoma tigrinum) from central Indiana. Their study documented a population size discrepancy in which the effective population size (Ne) estimate made from mitochondrial DNA (mtDNA) sequences exceeded that derived from six nuclear microsatellite loci. The authors provided three possible hypotheses that may explain this discrepancy: (1) Extreme variation in male, but not female, reproductive success. Such a large variance in male reproduction would reduce the male effective population size, thereby leading to a reduction in the microsatellite-derived Ne. (2) Male-biased dispersal and secondary contact among populations. The former would lead to mtDNA (but not nuclear DNA) population divergence. The latter would then admix, and thereby, enrich the diversity of the mtDNA pools. (3) Microsatellite size homoplasy. If left unaccounted for by the evolutionary model used in the analysis, excessive parallel and back mutations among the alleles would result in underestimates of the true genetic diversity of the microsatellite loci, and thereby, of their associated Ne.
During our survey of the literature, we encountered several cases of a similar population size discrepancy in tuna (genus Thunnus). In each case, the mtDNA estimate of Ne exceeds that made from the microsatellite data by at least a factor of 8, but usually by a factor of >100 (Table 1). These population size discrepancies are not dependent on our assumed mutation rates (μ), given both the magnitude of the deviations and our use of fast mtDNA and slow microsatellite μ for tuna. Our use of available fast mtDNA but slow microsatellite μ for tuna (Martinez et al., 2006, Riccioni et al., 2010) results in decreased and increased estimates of Ne, respectively, and thereby, conservative estimates of the population size discrepancies. Our rate of 4.9 × 10−8 substitutions per site per year (sub/site/yr) for the mitochondrial control region (CR) is ∼25% faster than the μ used in other tuna studies (e.g., 3.6 × 10−8 sub/site/yr; Carlsson et al., 2004). Furthermore, our population size discrepancies persist even if a faster CR μ estimated for other fishes (1.1 × 10−7 sub/site/yr; McMillan and Palumbi, 1997) is used instead of our fast tuna-specific μ (4.9 × 10−8 sub/site/yr). We then use a rate of 1.3 × 10−8 sub/site/yr for ATPase6/ATPase8, which is now widely accepted for fishes (Betancur-R and Armbruster, 2009, Santos et al., 2011), because it is based on a number of well-calibrated μ for diverse teleost groups (Bermingham et al., 1997). In turn, our microsatellite rate of 10−4 mutations per locus per generation (mut/loc/gen) is five times slower and thus more conservative than the microsatellite estimates of μ used in many other fish studies (e.g., 5 × 10−4 mut/loc/gen; Lippé et al., 2006).
This study uses Bayesian inference to document a similar population size discrepancy between the mtDNA- and microsatellite-derived estimates of Ne for two previously unstudied populations of Pacific Bluefin Tuna (T. orientalis) and Yellowfin Tuna (T. albacares). We then use phylogenetic character analyses of inferred genealogies to reveal similar reduced levels of mtDNA and microsatellite homoplasy. In light of these results, we reject the third hypothesis of Bos et al. (2008) for microsatellite size homoplasy and propose instead a more specific version of their second explanation that the population size discrepancy may be due to behavioral differences between the sexes and secondary contact among populations. We then call for more critical testing of our explanation with more local populations of tuna and with other groups (both animal and plant) that differ in their life history characteristics.
Section snippets
Methods
Hypervariable control region I (CRI) sequences were compiled for 28 individuals of Pacific Bluefin Tuna and 41 specimens of Pacific Yellowfin Tuna. These CRI were separately aligned with Clustal X (Thompson et al., 1997) to generate multiple sequence alignments of 249 base pairs (bp) for Pacific Bluefin Tuna and 331 bp for Yellowfin Tuna. These alignments included 53 sequences from Alvarado Bremer et al., 1997, Alvarado Bremer et al., 2005, Ely et al., 2005, Takashima et al., 2006, and Viñas and
Population size estimates
The mean estimates of Θ for the CRI datasets were 0.352 for Pacific Bluefin Tuna (median = 0.341, 95% HPD = 0.205–0.524) and 0.275 for Yellowfin Tuna (0.271, 0.176–0.388). As in any coalescent estimation with compound parameters such as Θ, the units of μ in a MIGRATE sequence analysis are in substitutions per site per generation (Beerli, 2008). Thus, we converted the fast CR rate of 4.9 × 10−8 sub/site/yr to 2.9 × 10−7 sub/site/gen for Pacific Bluefin Tuna and 1.7 × 10−7 sub/site/gen for Yellowfin Tuna
Acknowledgments
We thank G. Burleigh, B. Knudsen, M.R. Tennant, and Y.Wang for their suggestions about our study. PB was partly supported by NSF Grant DEB 0822626 and DEB 1145999.
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