Hybridization underlies localized trait evolution in cavefish

Abstract

Compared to selection on new mutations and standing genetic variation, the role of gene flow in generating adaptive genetic variation has been subject to much debate. Theory predicts that gene flow constrains adaptive evolution via natural selection by homogenizing allele frequencies among populations and introducing migrant alleles that may be locally maladaptive. However, recent work has revealed that populations can diverge even when high levels of gene flow are present and that gene flow may play an underappreciated role in facilitating local adaptation by increasing the amount of genetic variation present for selection to act upon. Here, we investigate how genetic variation introduced by gene flow contributes to adaptive evolution of complex traits using an emerging eco-evolutionary model system, the Mexican tetra (Astyanax mexicanus). The ancestral surface form of the Mexican tetra has repeatedly invaded and adapted to cave environments. The Chica cave is unique in that it contains several pool microenvironments inhabited by putative hybrids between surface and cave populations, providing an opportunity to investigate the dynamics of complex trait evolution and gene flow on a local scale. Here we conduct high-resolution genomic mapping and analysis of eye morphology and pigmentation in fish from multiple pools within Chica cave. We demonstrate that hybridization between cave and surface populations contributes to highly localized variation in behavioral and morphological traits. Analysis of sleep and locomotor behaviors between individual pools within this cave revealed reduced sleep associated with an increase in ancestry derived from cave populations, suggesting pool-specific ecological differences may drive the highly-localized evolution of sleep and locomotor behaviors. Lastly, our analyses uncovered a compelling example of convergent evolution in a core circadian clock gene in multiple independent cavefish lineages and burrowing mammals, indicating a shared genetic mechanism underlying circadian disruption in subterranean vertebrates. Together, our results provide insight into the evolutionary mechanisms that promote adaptive genetic variation and the genetic basis of complex behavioral phenotypes involved in local adaptation.

Phylogeographic relationships and morphological evolution between cave and surface Astyanax mexicanus populations (De Filippi 1853) (Actinopterygii, Characidae)

“…Our analysis revealed evidence of at least four historical events of ancestral gene flow between surface and cave populations, indicating multiple instances of introgression throughout their evolutionary history. This finding supports previous studies that emphasized the importance of gene flow in the evolutionary dynamics of cave populations, as observed in populations such as Chica and Pachón (Herman et al, 2018;Moran et al, 2022).…”

“…Three out of four migration events observed involve the cave populations from the Sierra de El Abra region, which have experienced invasions by surface fish at different times (Figure 3a). The most recent migration event was estimated at the southern part of the Sierra de El Abra region, where Chica, Chiquitita and Toro were connected with surface populations of Lineage 1 from the Pánuco basin, as documented in Moran et al (2022). At the northern limit of the Sierra de El Abra, gene flow was detected between the ancestral surface lineage and Pachón cave, which is interesting since ADMIXTURE analysis did not indicate recent hybrids within Pachón cave.…”

“…Cave populations from Lineage 2 were assigned to four different genetic clusters. Cave populations of Chica, Chiquitita and Toro formed a genetic cluster (Clade 2D, Figure 2b) with evidence of admixture with the surface Pánuco basin populations from Lineage 1 (Clade 1B) (similar to Moran et al, 2022), as well as with other cave populations of Sierra de El Abra. Most cave populations from the Sierra de El Abra region were grouped on a different cluster (Clade 2C) with some evidence of admixture with both Pánuco basin and Subterráneo cave populations (Clade 1B and Clade 1C).…”

“…Genomes were downsampled to match the RADseq loci, and only the RADseq loci were analysed. A companion paper (Moran et al, 2022) provides an in-depth analysis of WGS data.…”

“…In addition, our results showed admixture between the Chica group and the Sierra de El Abra cave populations, as well as with surface populations of Lineage 1. This admixture could be influencing the differentiation observed for the Chica group (see Moran et al, 2022).…”