Complex hybridization between deeply diverged fish species in a disturbed ecosystem

Abstract

Over the past two decades researchers have documented the extent of natural hybridization between closely related species using genomic tools. Many species across the tree of life show evidence of past hybridization with their evolutionary relatives. In some cases, this hybridization is complex, involving gene flow between more than two species. While hybridization is common over evolutionary timescales, some researchers have proposed that it may be even more common in contemporary populations where anthropogenic disturbance has modified myriad aspects of the environments in which organisms live and reproduce. Here, we develop a flexible tool for local ancestry inference in hybrids derived from three source populations and describe a complex, recent hybridization event between distantly related swordtail fish lineages (Xiphophorus) and its potential links to anthropogenic disturbance.

Semipermeable species boundaries create opportunities for gene flow and adaptive potential

“…This pattern could be due to the life history characteristics of the species and/or selection. The simplest explanation is that F. polyctena or F. rufa queens are forced to mate with F. aquilonia males due to a lack of conspecifics, because of differences in their abundance in Finland (Seifert, 2018), similarly to swordtail fish three‐way hybridisation in Mexico (Banerjee et al, 2022). A complementary explanation is that since highly supercolonial F. aquilonia mates on top of or close to its nest (Seifert, 2018), workers protect the queens from nonconspecifics, as has been observed in other ant species (Eyer et al, 2023; Staab & Kleineidam, 2014).…”

“…Our findings are among the few that pertain to a mosaic hybrid zone involving multiple species. We add a new system to the groups of taxa exhibiting natural mosaic hybrid zones (Abbott & Brennan, 2014;Fraïsse et al, 2014;Rieseberg et al, 1999) and multispecies hybridisation (Banerjee et al, 2022;Grant & Grant, 2020;Heliconius Genome Consortium, 2012;Natola et al, 2022;Ottenburghs, 2019;Reutimann et al, 2020).…”

Extensive hybridisation between multiple differently adapted species may aid persistence in a changing climate

“…This pattern could be caused by life history characteristics of the species and/or due to selection. The simplest explanation is that F. polyctena or F. rufa queens are forced to mate with F. aquilonia males due to lack of conspecifics, because of differences in abundance in Finland (Seifert, 2018), similarly as has been suggested with swordtail fish three-way hybridisation (Banerjee et al, 2022). A complementary explanation is that since highly supercolonial F. aquilonia mates on top of or close to its nest (Seifert, 2018), workers protect the queens from nonconspecifics.…”

“…Our findings are among the few where the mosaic hybrid zone is formed among multiple species. We add a new system to the groups of taxa exhibiting natural mosaic hybrid zones (Abbott & Brennan, 2014;Fraïsse et al, 2014;Rieseberg et al, 1999) and multi-species hybridisation (Banerjee et al, 2022;Grant & Grant, 2020;Heliconius Genome Consortium, 2012;Natola et al, 2022;Ottenburghs, 2019;Reutimann et al, 2020).…”

“…Hybridisation is commonly investigated between two species. However, multi-species hybridisation has been documented from white oaks (Reutimann et al, 2020) to birds (Grant & Grant, 2020;Natola et al, 2022;Ottenburghs, 2019), fish (Banerjee et al, 2022), and butterflies (Heliconius Genome Consortium, 2012). Multi-species hybridisation is likely to be more frequent in sympatric groups with a low degree of reproductive isolation, and one species may act as a "conduit" species and a vehicle of gene flow between two otherwise isolated species (Grant & Grant, 2020).…”