Phylogeographic relationships and morphological evolution between cave and surface Astyanax mexicanus populations (De Filippi 1853) (Actinopterygii, Characidae)
Marco Garduño‐Sánchez,
Jorge Hernández‐Lozano,
Rachel L. Moran
et al.
Abstract:The Astyanax mexicanus complex includes two different morphs, a surface‐ and a cave‐adapted ecotype, found at three mountain ranges in Northeastern Mexico: Sierra de El Abra, Sierra de Guatemala and Sierra de la Colmena (Micos). Since their discovery, multiple studies have attempted to characterize the timing and the number of events that gave rise to the evolution of these cave‐adapted ecotypes. Here, using RADseq and genome‐wide sequencing, we assessed the phylogenetic relationships, genetic structure and ge… Show more
“…1 ). The timing and the number of independent colonization events that gave rise to the cavefish populations is a matter of debate, but most recent studies point to a relatively recent origin (20,000 to 200,000 years) and few independent events (2 to 4) [ 7 – 10 ]. Fig.…”
Background
Several studies suggested that cavefish populations of Astyanax mexicanus settled during the Late Pleistocene. This implies that the cavefish’s most conspicuous phenotypic changes, blindness and depigmentation, and more cryptic characters important for cave life, evolved rapidly.
Results
Using the published genomes of 47 Astyanax cavefish from la Cueva de El Pachón, El Sótano de la Tinaja, La Cueva Chica and El Sótano de Molino, we searched for putative loss-of-function mutations in previously defined sets of genes, i.e., vision, circadian clock and pigmentation genes. Putative non-functional alleles for four vision genes were identified. Then, we searched genome-wide for putative non-functional alleles in these four cave populations. Among 512 genes with segregating putative non-functional alleles in cavefish that are absent in surface fish, we found an enrichment in visual perception genes. Among cavefish populations, different levels of shared putative non-functional alleles were found. Using a subset of 12 genes for which putative loss-of-function mutations were found, we extend the analysis of shared pseudogenes to 11 cave populations. Using a subset of six genes for which putative loss-of-function mutations were found in the El Sótano del Toro population, where extensive hybridization with surface fish occurs, we found a correlation between the level of eye regression and the amount of putative non-functional alleles.
Conclusions
We confirm that very few putative non-functional alleles are present in a large set of vision genes, in accordance with the recent origin of Astyanax mexicanus cavefish. Furthermore, the genome-wide analysis indicates an enrichment of putative loss-of-function alleles in genes with vision-related GO-terms, suggesting that visual perception may be the function chiefly impacted by gene losses related to the shift from a surface to a cave environment.
The geographic distribution of putative loss-of-function alleles newly suggests that cave populations from Sierra de Guatemala and Sierra de El Abra share a common origin, albeit followed by independent evolution for a long period. It also supports that populations from the Micos area have an independent origin. In El Sótano del Toro, the troglomorphic phenotype is maintained despite massive introgression of the surface genome.
“…1 ). The timing and the number of independent colonization events that gave rise to the cavefish populations is a matter of debate, but most recent studies point to a relatively recent origin (20,000 to 200,000 years) and few independent events (2 to 4) [ 7 – 10 ]. Fig.…”
Background
Several studies suggested that cavefish populations of Astyanax mexicanus settled during the Late Pleistocene. This implies that the cavefish’s most conspicuous phenotypic changes, blindness and depigmentation, and more cryptic characters important for cave life, evolved rapidly.
Results
Using the published genomes of 47 Astyanax cavefish from la Cueva de El Pachón, El Sótano de la Tinaja, La Cueva Chica and El Sótano de Molino, we searched for putative loss-of-function mutations in previously defined sets of genes, i.e., vision, circadian clock and pigmentation genes. Putative non-functional alleles for four vision genes were identified. Then, we searched genome-wide for putative non-functional alleles in these four cave populations. Among 512 genes with segregating putative non-functional alleles in cavefish that are absent in surface fish, we found an enrichment in visual perception genes. Among cavefish populations, different levels of shared putative non-functional alleles were found. Using a subset of 12 genes for which putative loss-of-function mutations were found, we extend the analysis of shared pseudogenes to 11 cave populations. Using a subset of six genes for which putative loss-of-function mutations were found in the El Sótano del Toro population, where extensive hybridization with surface fish occurs, we found a correlation between the level of eye regression and the amount of putative non-functional alleles.
Conclusions
We confirm that very few putative non-functional alleles are present in a large set of vision genes, in accordance with the recent origin of Astyanax mexicanus cavefish. Furthermore, the genome-wide analysis indicates an enrichment of putative loss-of-function alleles in genes with vision-related GO-terms, suggesting that visual perception may be the function chiefly impacted by gene losses related to the shift from a surface to a cave environment.
The geographic distribution of putative loss-of-function alleles newly suggests that cave populations from Sierra de Guatemala and Sierra de El Abra share a common origin, albeit followed by independent evolution for a long period. It also supports that populations from the Micos area have an independent origin. In El Sótano del Toro, the troglomorphic phenotype is maintained despite massive introgression of the surface genome.
Astyanax mexicanus offers a unique model for studying parallel evolution, with cave-dwelling forms arising from at least two distinct surface lineages. Here, we examined repeated evolution in the two cave-adapted lineages across four phenotypic datasets: (i) meristic data; (ii) ecomorphological data; and geometric morphometric data for (iii) head and (iv) premaxillary bone shape. Additionally, we assessed the association of these phenotypes with their phylogenetic history. Certain traits exhibited evidence of parallel evolution for the cave ecotype across lineages, such as increased maxillary tooth count, reduced lateral line scale count, and shorter ascending process of the premaxillary bone. Geometric morphometric data showed a phenotypic divergence gradient in head shape between cave and surface populations, with the strongest divergence between Sierra de El Abra and surface populations and with less differentiation between surface populations and caves from Sierra de Guatemala and Micos. Cave populations that hybridize with surface populations (e.g. Micos) displayed the greatest overlap with the surface ecotype. There was a similar divergence gradient for premaxillary bone shape, but with weaker differentiation between cave and surface ecotypes. This evidence of repeated evolution in several cave traits emphasizes the significance of selective pressures exerted by the environment on the evolution of cave ecotypes.
Many species are paraphyletic, but current taxonomic practices often do not recognize this, and attempts are made to apply a monophyletic species concept. While allowing the recognition of ecomorphologically equivalent, or even phenotypically indistinguishable allopatric, taxa as species, this often leads to combining distinctive local forms (such as cave-adapted populations) or even whole adaptive radiations (often in lakes) with widespread paraphyletic species to force species monophyly. It is suggested that this has negative consequences for our documentation and understanding of biodiversity, as well as for conservation, through issues such as lack of IUCN red-listing.
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