Ornelas-Garcia, P. | Search bioRxiv

bioRxiv2021

Hybridization underlies localized trait evolution in cavefish

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 maladaptive1. However, recent work has revealed that populations can diverge even when high levels of gene flow are present2-4 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 upon5-8. 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 populations9, 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.

evolutionary biology↗

bioRxiv2020

A mutation in monoamine oxidase (MAO) affects the evolution of stress behavior in the blind cavefish Astyanax mexicanus

The neurotransmitter serotonin controls a great variety of physiological and behavioral processes. In humans, mutations affecting the monoamine oxidase or MAO, the serotonin-degrading enzyme, are highly deleterious. Yet, blind cavefish of the species A. mexicanus carry a partial loss-of-function mutation in MAO (P106L) and seem to thrive in their subterranean environment. Here, we established 4 fish lines, corresponding to the blind cave-dwelling and the sighted river-dwelling morphs of this species, with or without the mutation, in order to decipher the exact contribution of mao P106L in the evolution of cavefish neuro-behavioral traits. Unexpectedly, although mao P106L appeared as an excellent candidate for the genetic determinism of the loss of aggressive and schooling behaviors in cavefish, we demonstrated that it was not the case. Similarly, the anatomical variations in monoaminergic systems observed between cavefish and surface fish brains were independent from mao P106L, and rather due other, morph-dependent developmental processes. On the other hand, we found that mao P106L strongly affected anxiety-like behaviors. Cortisol measurements showed lower basal levels and an increased amplitude of stress response after a change of environment in fish carrying the mutation. Finally, we studied the distribution of the P106L mao allele in wild populations of cave and river A. mexicanus, and discovered that the mutant allele was present - and sometimes fixed - in all populations inhabiting caves of the Sierra de El Abra. The possibility that this partial loss-of-function mao allele evolves under a selective or a genetic drift regime in the particular cave environment is discussed.

neuroscience↗