Genomic data and multi-species demographic modelling uncover past hybridization between currently allopatric freshwater species

Abstract

11In freshwater fish, processes of population divergence and speciation are often linked 12 to the geomorphology of rivers and lakes that create barriers isolating populations. 13However, current geographical isolation does not necessarily imply total absence of 14 gene flow during the divergence process. Here, we focused on four species of the 15 genus Squalius in Portuguese rivers: S. carolitertii, S. pyrenaicus, S. aradensis and S. 16 torgalensis. Previous studies based on eight nuclear and mitochondrial markers 17 revealed incongruent patterns, with nuclear loci suggesting that S. pyrenaicus was a 18 paraphyletic group, since its northern populations were genetically closer to S. 19 carolitertii than to other southern populations. Here, for the first time, we successfully 20 applied a genomic approach to the study of the relationship between these species, 21 using a Genotyping by Sequencing approach to obtain single nucleotide 22 polymorphisms (SNPs). Our results revealed a species tree with two main lineages: (i) 23 S. carolitertii and S. pyrenaicus; (ii) S. torgalensis and S. aradensis. Moreover, 24 regarding S. carolitertii and S. pyrenaicus, we found evidence for past introgression 25 between these two species in the northern part of S. pyrenaicus distribution. This 26 introgression reconciles previous mitochondrial and nuclear incongruent results and 27 explains the apparent paraphyly of S. pyrenaicus. Although we cannot distinguish a 28 scenario of hybrid speciation from secondary contact, our estimates are consistent 29 across models, suggesting that the northern populations of S. pyrenaicus received 30 approximately 80% from S. carolitertii and 20% from southern S. pyrenaicus. This 31 illustrates that even in freshwater species currently found in isolated river drainages, 32we are able to detect past gene flow events in present-day genomes, suggesting that 33 speciation is more complex than simply allopatric. 34 35 3

Historical biogeography of the Iberian Peninsula: multilocus phylogeny and ancestral area reconstruction for the freshwater fish genus Squalius (Actinopterygii, Leuciscidae)

“…Considering the evidence shown here, the two hypotheses regarding mitonuclear discordance in S. pyrenaicus are not mutually exclusive: mitochondrial and nuclear introgression could both contribute to the reticulate pattern found in the Tagus Basin (Mendes et al, 2019). Further studies considering a broader genomic scale would help to elucidate the nature of the mitonuclear discordance.…”

Complex introgression among three diverged largemouth bass lineages

“…While significant, this differentiation is still much lower than that observed between Florida Bass (FLB) and NLB (F ST = 0.749, 1807 fixed unlinked nuclear SNPs, 19 fixed ND2 SNPs). These values are higher than those observed using GBS SNPs for different species of Squalius chubs (F ST = 0.126–0.414) and comparable to F ST between diverged lineages of walleye (0.805; Mendes et al, 2021; Zhao et al, 2020). Our results contribute to a growing scientific consensus around the validity of M .…”