Mitochondrial DNA paradox: sex-specific genetic structure in a marine mussel – despite maternal inheritance and passive dispersal

Abstract

BackgroundWhen genetic structure is identified using mitochondrial DNA (mtDNA), but no structure is identified using biparentally-inherited nuclear DNA, the discordance is often attributed to differences in dispersal potential between the sexes.ResultsWe sampled the intertidal rocky shore mussel Perna perna in a South African bay and along the nearby open coast, and sequenced maternally-inherited mtDNA (there is no evidence for paternally-inherited mtDNA in this species) and a biparentally-inherited marker. By treating males and females as different populations, we identified significant genetic structure on the basis of mtDNA data in the females only.ConclusionsThis is the first study to report sex-specific differences in genetic structure based on matrilineally-inherited mtDNA in a passively dispersing species that lacks social structure or sexual dimorphism. The observed pattern most likely stems from females being more vulnerable to selection in habitats from which they did not originate, which also manifests itself in a male-biased sex ratio. Our results have three important implications for the interpretation of population genetic data. First, even when mtDNA is inherited exclusively in the female line, it also contains information about males. For that reason, using it to identify sex-specific differences in genetic structure by contrasting it with biparentally-inherited markers is problematic. Second, the fact that sex-specific differences were found in a passively dispersing species in which sex-biased dispersal is unlikely highlights the fact that significant genetic structure is not necessarily a function of low dispersal potential or physical barriers. Third, even though mtDNA is typically used to study historical demographic processes, it also contains information about contemporary processes. Higher survival rates of males in non-native habitats can erase the genetic structure present in their mothers within a single generation.

Dispersal barriers and stochastic reproductive success do not explain small-scale genetic structure in a broadcast spawning marine mussel

“…These sequences have been submitted to GenBank (accession numbers KC356872-KC357249). We compared the new sequences with 172 previously published se quences from adult P. perna (Nicastro et al 2008, Teske et al 2012. Genetic diversity indices in P. perna were mostly larger for the samples from the bay than those from the open coast, with the difference being particularly clear in the adult females (Table 1).…”

“…We have previously suggested that the skewed sex ratio in Perna perna could be the result of post-settlement selection (Teske et al 2012). Females have greater reproductive output than males ), and mussels in bays produce more gametes than those on the open coast (McQuaid & Phillips 2006).…”

“…DNA was extracted from foot tissue in the 3 molluscs and from cirri in C. dentatus using the CTAB extraction protocol (Doyle & Doyle 1990). The mitochondrial COI gene was amplified as described previously (Nicastro et al 2008); it is matrilineally inherited in all 4 species (Weber et al 2009, Teske et al 2012). Levels of haplotype and nucleotide diversity were determined in DnaSP v5.10.01 (Librado & Rozas 2009).…”

“…To compare genetic diversity in the species with separate sexes (P. perna) with that of hermaphrodites (all others), a data set was created from previously published data (Teske et al 2012) that combined equal numbers of COI sequences from males and females from each site (Adults a in Table 1). We also used this data set and a second one (Adults b in Table 1) in which the number of sequences from male and female mussels reflected empirical sex ratios (coast: 3.8 males:1 female; bay: 1.2 males:1 female; Teske et al 2012) to compare genetic diversity in adults and juveniles of P. perna. The latter could not be sexed due to the absence of gonads.…”

Does population genetic structure support present management regulations of the northern shrimp (Pandalus borealis) in Skagerrak and the North Sea?

“…Structure between fjords/bays and open coast has also been found in other organisms (e.g. mussels: Nicastro et al, 2008, Teske et al, 2012, including cod in the Skagerrak region (Knutsen et al, 2011). Oceanographic features, such as bathymetry, temperature, and salinity boundaries, and habitat heterogeneity may all act as barriers to population connectivity in marine species in this region (e.g.…”