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Morphology, molecules and taxonomy: extreme incongruence in pleurocerids ( G astropoda, C erithioidea, P leuroceridae)
Author(s) -
Whelan Nathan V.,
Strong Ellen E.
Publication year - 2016
Publication title -
zoologica scripta
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.204
H-Index - 64
eISSN - 1463-6409
pISSN - 0300-3256
DOI - 10.1111/zsc.12139
Subject(s) - biology , mitochondrial dna , pseudogene , genetics , species complex , polyphyly , evolutionary biology , non mendelian inheritance , haplotype , population , nuclear gene , haplogroup , clade , gene , genome , phylogenetics , allele , phylogenetic tree , demography , sociology
Pronounced mitochondrial heterogeneity within putative species of P leuroceridae has prevented meaningful systematic revisions of this critically imperilled freshwater family. Previous studies have demonstrated that this mitochondrial diversity often produces polyphyletic species on mitochondrial gene trees, but its significance is unclear. Hypotheses advanced to explain this pattern have included cryptic species, retained ancestral polymorphisms and introgression; other possible explanations such as doubly uniparental inheritance or the presence of pseudogenes have not been given due consideration. Previous analyses have not included adequate sampling, neither in terms of number of individuals nor in geographic coverage, to adequately test any of these hypotheses. To fully characterize mitochondrial heterogeneity in pleurocerids and robustly assess possible causal explanations, we collected 239 individuals representing four putative species from seven sites and sequenced the COI and 16S rRNA mitochondrial genes and the H 3 nuclear gene for all individuals. We also used whole‐genome shotgun sequencing to construct and annotate a mitochondrial genome for one individual. Characters with demonstrated utility in morphospecies delineation of gastropods (head–foot coloration, shell and radular morphology, pallial oviduct anatomy) were examined for a subset of individuals to determine whether morphology co‐varied by haplotype clade. We found pronounced mitochondrial heterogeneity at both the population level and species level in three of the species examined, but our data reject paralogous nuclear copies of mitochondrial genes ( NUMT s) and doubly uniparental inheritance as causal mechanisms, and there was no evidence of cryptic diversity. Mutation rates were found to differ significantly among mitochondrial lineages, and population genetic statistics revealed a signature of balancing selection that could be acting to maintain this diversity. The observed pattern is similar to that seen in lineages with inherited endosymbionts like Wolbachia infections, which merits further investigation. Although questions remain concerning the precise cause(s) of intraspecific mitochondrial diversity in pleurocerids, nuclear and/or genomic data, combined with anatomical and life history investigations in an integrative phylogenetic context, is the most promising avenue for resolving pleurocerid systematics.