Unraveling historical introgression and resolving phylogenetic discord within Catostomus (Osteichthys: Catostomidae)

Abstract

Background: Porous species boundaries can be a source of conflicting hypotheses, particularly when coupled with variable data and/or methodological approaches. Their impacts can often be magnified when non-model organisms with complex histories of reticulation are investigated. One such example is the genus Catostomus (Osteichthys, Catostomidae), a freshwater fish clade with conflicting morphological and mitochondrial phylogenies. The former is hypothesized as reflecting the presence of admixed genotypes within morphologically distinct lineages, whereas the latter is interpreted as the presence of distinct morphologies that emerged multiple times through convergent evolution. We tested these hypotheses using multiple methods, to including multispecies coalescent and concatenated approaches. Patterson's D-statistic was applied to resolve potential discord, examine introgression, and test the putative hybrid origin of two species. We also applied naïve binning to explore potential effects of concatenation. Results: We employed 14,007 loci generated from ddRAD sequencing of 184 individuals to derive the first highly supported nuclear phylogeny for Catostomus. Our phylogenomic analyses largely agreed with a morphological interpretation,with the exception of the placement of Xyrauchen texanus, which differs from both morphological and mitochondrial phylogenies. Additionally, our evaluation of the putative hybrid species C. columbianus revealed a lack introgression and instead matched the mitochondrial phylogeny. Furthermore, D-statistic tests clarified all discrepancies based solely on mitochondrial data, with agreement among topologies derived from concatenation and multispecies coalescent approaches. Extensive historic introgression was detected across six species-pairs. Potential endemism in the Virgin and Little Colorado Rivers was also apparent, and the former genus Pantosteus was derived as monophyletic, save for C. columbianus. Conclusions: Complex reticulated histories detected herein support the hypothesis that introgression was responsible for conflicts that occurred within the mitochondrial phylogeny, and explains discrepancies found between it and previous morphological phylogenies. Additionally, the hybrid origin of C. columbianus was refuted, but with the caveat that more fine-grain sampling is still needed. Our diverse phylogenomic approaches provided largely concordant results, with naïve binning useful in exploring the single conflict. Considerable diversity was found within Catostomus across southwestern North America, with two drainages [Virgin River (UT) and Little Colorado River (AZ)] reflecting unique composition.