Astyanax mexicanus surface and cavefish chromosome-scale assemblies for trait variation discovery

Abstract

The ability of organisms to adapt to sudden extreme environmental changes produces some of the most drastic examples of rapid phenotypic evolution. The Mexican Tetra, Astyanax mexicanus, is abundant in the surface waters of northeastern Mexico, but repeated colonizations of cave environments have resulted in the independent evolution of troglomorphic phenotypes in several populations. Here, we present three chromosome-scale assemblies of this species, for one surface and two cave populations, enabling the first whole-genome comparisons between independently evolved cave populations to evaluate the genetic basis for the evolution of adaptation to the cave environment. Our assemblies represent the highest quality of sequence completeness with predicted protein-coding and noncoding gene metrics far surpassing prior resources and, to our knowledge, all long-read assembled teleost genomes, including zebrafish. Whole-genome synteny alignments show highly conserved gene order among cave forms in contrast to a higher number of chromosomal rearrangements when compared with other phylogenetically close or distant teleost species. By phylogenetically assessing gene orthology across distant branches of amniotes, we discover gene orthogroups unique to A. mexicanus. When compared with a representative surface fish genome, we find a rich amount of structural sequence diversity, defined here as the number and size of insertions and deletions as well as expanding and contracting repeats across cave forms. These new more complete genomic resources ensure higher trait resolution for comparative, functional, developmental, and genetic studies of drastic trait differences within a species.

Keywords: Astyanax mexicanus; cavefish; chromosome assembly.

Fig. 1.

Summary of interspecies chromosomal synteny. a) Geographical representation of the independent cave morph populations and their physical appearance used in this study. Image courtesy of Alex Keene. b) Gene ortholog synteny of A. mexicanus against three teleost species. c) Higher-resolution image of A. mexicanus (surface genome) aligned to the same three teleost species in B.

Fig. 2.

Summary of OrthoFinder analysis of vertebrate species A. mexicanus, D. rerio, O. latipes, X. maculatus, L. oculatus, P. textilis, P. muralis, G. gallus, H. sapiens, P. troglodytes, M. musculus, R. norvegicus, M. domestica, X. tropicalis, and C. intestinalis. Bar charts describe data for each species, aligned to the matching species in the tree. a) Phylogenetic tree built with all species using shared gene orthologs. b) Number of orthogroups each classified by type per species. c) Percentage of genes by orthogroups by species. d) Number of species-specific orthogroups per species. e) Ortholog multiplicities for all species.

Fig. 3.

Genomic SV among A. mexicanus cave morph assemblies when compared with surface. Cave morph-specific distribution by counts for a) Molino, b) Tinaja, and c) Pachón for the size distribution of 500–10,000 bp.