History repeated: recent and historical mitochondrial introgression between the current darter Etheostoma uniporum and rainbow darter Etheostoma caeruleum (Teleostei: Percidae)

Abstract

Incongruence between recognized taxonomy and phylogenetic relationships between two species from a diverse clade (Percidae: Etheostomatinae) of stream fishes was found in a mitochondrial (mt) DNA gene tree. Two darters in subgenus Oligocephalus, Etheostoma uniporum current darter and Etheostoma caeruleum rainbow darter were sampled throughout their sympatric distribution in the Ozark Highlands of the central United States. Sequences from cytochrome (cyt) b and the first intron of the nuclear marker S7 were analysed separately using maximum parsimony and Bayesian methods. Cyt b recovered both species as polyphyletic; E. uniporum haplotypes were interspersed within E. caeruleum. However, both species were monophyletic and non-sister taxa based on S7. The cyt b gene tree pattern is caused by introgressive hybridization resulting in the mtDNA replacement of E. uniporum haplotypes by those of E. caeruleum. Some E. uniporum haplotypes are shared with geographically proximate E. caeruleum, and this is consistent with recent hybridization, while other E. uniporum haplotypes indicate historical sorting of introgressed lineages. The mechanism of introgression is likely asymmetric sneaking behaviour by male E. uniporum, a mating tactic observed in related species. MtDNA replacement may have occurred in E. uniporum due to drift fixation in a historically small female effective population. Additional evidence for darter hybridization will likely be discovered in future molecular genetic surveys of the nearly 200 species in eastern North America.

Low genetic diversity and small long-term population sizes in the spring endemic watercress darter, Etheostoma nuchale

“…Although incomplete lineage sorting cannot be completely ruled out, it is unlikely the main explanation for the close relationship among RS E. nuchale and WC E. swaini based on mtDNA. Mitochondrial introgression and replacement as a result of historical or ongoing hybridization has become increasingly recognized not only for members of the E. asprigene species group (Lang and Mayden 2007;Ray et al 2008) but also among other darter species (Bossu and Near 2009;Keck and Near 2009). Thus, we conclude that the current taxonomic status of E. nuchale is valid.…”

“…All base assignments were confirmed visually using Sequencher 4.2 (Gene Codes) and alignments were made by eye in BioEdit (Hall 1999). Heterozygous positions detected in S7 sequences were coded as ambiguous based on standard nomenclature of the IUPAC (Domingues et al 2005;Ray et al 2008). A total of 223 specimens (144 E. nuchale and 79 E. swaini; Table 1) were genotyped for nine microsatellite loci using primers designed for a close relative, E. caeruleum (Eca10EPA, Eca11EPA, Eca22EPA, Eca36EPA, Eca 37EPA, Eca46EPA, Eca48EPA, Eca49EPA, and Eca71 EPA; Tonnis 2006).…”

AFLPs support deep relationships among darters (Percidae: Etheostomatinae) consistent with morphological hypotheses

“…Previous research using mtDNA and nuclear introns has not been able to fully resolve the darter phylogeny, and different genetic markers have yielded phylogenetic and morphological discordance; for example, the phylogenetic position of Ammocrypta, and the relationship of Etheostoma zonale to snubnose darters (Wood and Mayden, 1997;Song et al, 1998;Sloss et al, 2004;Keck and Near, 2008;Mendelson and Wong, 2010). Many sympatric darter species have been found to share haplotypes because of hybridization and mitochondrial replacement, confounding phylogenetic analyses (Ray et al, 2008;Bossu and Near, 2009;Keck and Near, 2010).…”

Phylogeny and phylogeography of Altolamprologus: ancient introgression and recent divergence in a rock-dwelling Lake Tanganyika cichlid genus

“…Lamprologine species can produce interspecific offspring for long periods of time following their divergence (Koblmüller et al, 2007b;Sturmbauer et al, 2010), which may explain the frequency of interspecific introgressions detected in this group. When small population size contributes to rapid sorting of lineages, as in A. compressiceps, mitochondrial replacement by the introgressed lineage is not an altogether unlikely outcome (Leonard et al, 2007;Ray et al, 2007).…”