Prevalent Introgression Underlies Convergent Evolution in the Diversification ofPungitiusSticklebacks

Abstract

New mutations and standing genetic variations contribute significantly to repeated phenotypic evolution in sticklebacks. However, less is known about the role of introgression in this process. We analysed taxonomically and geographically comprehensive genomic data from Pungitius sticklebacks to decipher the extent of introgression and its consequences for the diversification of this genus. Our results demonstrate that introgression is more prevalent than suggested by earlier studies. Although gene flow was generally bidirectional, it was often asymmetric and left unequal genomic signatures in hybridizing species, which might, at least partly, be due to biased hybridization and/or population size differences. In several cases, introgression of variants from one species to another was accompanied by transitions of pelvic and/or lateral plate structures – important diagnostic traits in Pungitius systematics – and frequently left signatures of adaptation in the core gene regulatory networks of armor trait development. This finding suggests that introgression has been an important source of genetic variation and enabled phenotypic convergence among Pungitius sticklebacks. The results highlight the importance of introgression of genetic variation as a source of adaptive variation underlying key ecological and taxonomic traits. Taken together, our study indicates that introgression-driven convergence likely explains the longstanding challenges in resolving the taxonomy and systematics of this small but phenotypically highly diverse group of fish.

Estimating recent and historical effective population size of marine and freshwater sticklebacks

“…What makes it particularly interesting in the context of N e estimation is its presence in both open marine habitats as well as in landlocked freshwater habitats. Previous studies have also found evidence for ancient and potentially ongoing introgression in some parts of its distribution range (Guo et al, 2019;Feng et al, 2022;Y. Wang et al, 2023).…”

Secondary Contact, Introgressive Hybridization, and Genome Stabilization in Sticklebacks

“… Dowling and Secor 1997 ; Harrison and Larson 2014 ; Suarez-Gonzalez et al 2018 ), including humans ( Huerta-Sánchez et al 2014 ; Sankararaman et al 2014 , 2016 ). There is also well-documented evidence of introgression fueling adaptation in several species ( Hedrick 2013 ; Racimo et al 2015 ; Marques et al 2019 ; Wang et al 2023 ). However, amidst this process of introgression of adaptive and neutral variants, there exists a genome-wide selection against hybrids (e.g.…”

Secondary contact, introgressive hybridization and genome stabilization in sticklebacks

“…Dowling & Secor, 1997; Harrison & Larson, 2014; Suarez-Gonzalez et al, 2018), including humans (Huerta-Sánchez et al, 2014; Sankararaman et al, 2014, 2016). There is also well-documented evidence of introgression fueling adaptation in several species (Hedrick, 2013; Marques et al, 2019; Racimo et al, 2015; Wang et al, 2023). However, amidst this process of introgression of adaptive and neutral variants, there exists a genome-wide selection against hybrids (e.g.…”