Dataset Information

Regressive evolution in the Mexican cave tetra, Astyanax mexicanus.

ABSTRACT: The evolutionary forces driving the reduction of eyes and pigmentation in cave-adapted animals are unknown; Darwin famously questioned the role of natural selection in eye loss in cave fishes: "As it is difficult to imagine that eyes, although useless, could be in any way injurious to animals living in darkness, I attribute their loss wholly to disuse"[1]. We studied the genetics of eye and pigmentation regression in the Mexican cave tetra, Astyanax mexicanus, by mapping and quantitative trait loci (QTL) analysis. We also mapped QTL for the putatively constructive traits of jaw size, tooth number, and numbers of taste buds. The data suggest that eyes and pigmentation regressed through different mechanisms. Cave alleles at every eye or lens QTL we detected caused size reductions, consistent with evolution by natural selection but not with drift. QTL polarities for melanophore number were mixed, however, consistent with genetic drift. Arguments against a role for selection in the regression of cave-fish eyes cited the insignificant cost of their development [2, 3], but we argue that the energetic cost of their maintenance is sufficiently high for eyes to be detrimental in the cave environment. Regression can be caused either by selection or drift.

SUBMITTER: Protas M

PROVIDER: S-EPMC2570642 | biostudies-literature | 2007 Mar

REPOSITORIES: biostudies-literature

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Regressive evolution in the Mexican cave tetra, Astyanax mexicanus.

Protas Meredith M Conrad Melissa M Gross Joshua B JB Tabin Clifford C Borowsky Richard R

Current biology : CB 20070215 5

The evolutionary forces driving the reduction of eyes and pigmentation in cave-adapted animals are unknown; Darwin famously questioned the role of natural selection in eye loss in cave fishes: "As it is difficult to imagine that eyes, although useless, could be in any way injurious to animals living in darkness, I attribute their loss wholly to disuse"[1]. We studied the genetics of eye and pigmentation regression in the Mexican cave tetra, Astyanax mexicanus, by mapping and quantitative trait l ...[more]

PMID: 17306543

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Project description:BackgroundThe Mexican tetra (Astyanax mexicanus) has emerged as a good animal model to study the constructive and regressive changes associated with living in cave environments, as both the ancestral sighted morph and the cave dwelling morph are extant. The cave dwelling morphs lack eyes and body pigmentation, but have well developed oral and sensory systems that are essential for survival in dark environments. The cave forms and surface forms are interfertile and give rise to F1 hybrids progeny known as intermediates. In cavefish, degeneration of the lens is one of the key events leading to eye regression. We have previously shown that surgical lens removal in surface fish embryos has an effect on the craniofacial skeleton. Surprisingly, lens removal was also found to have an effect on the caudal teeth in the lower jaw. In order to understand this result, we analyzed the lower jaw and upper jaw dentitions of surface, cavefish and F1 hybrids of surface and cavefish and compared our findings with surface fish that underwent lens removal. We also investigated the upper jaw (premaxillae and maxillae) dentition in these fish.ResultsOur tooth analyses shows that cavefish have the highest numbers of teeth in the mandible and maxillae, surface forms have the lowest numbers and F1 hybrids are between these groups. These differences are not observed in the premaxillae. A wide diversity of cuspal morphology can also be found in these fish. Jaw size also differs amongst the groups, with the mandible exhibiting the greatest differences. Interestingly, tooth number in surgery fish is different only in the caudal region of the mandible; this is the region that is constrained in size in all morphs.ConclusionOur data provides the first detailed description of the jaw dentitions of two morphs of Astyanax mexicanus, as well as in F1 hybrids. Tooth number, patterning and cuspal morphology are enhanced in cavefish in all jaws. This is in contrast to the increase in tooth number previously observed on the lens ablated side of the surgery fish. These findings indicate that the mechanisms which govern the constructive traits in cavefish are different to the mechanisms causing an increase tooth number in surgery fish.

Project description:Numerous organisms around the globe have successfully adapted to subterranean environments. A powerful system in which to study cave adaptation is the freshwater characin fish, Astyanax mexicanus. Prior studies in this system have established a genetic basis for the evolution of numerous regressive traits, most notably vision and pigmentation reduction. However, identification of the precise genetic alterations that underlie these morphological changes has been delayed by limited genetic and genomic resources. To address this, we performed a transcriptome analysis of cave and surface dwelling Astyanax morphs using Roche/454 pyrosequencing technology. Through this approach, we obtained 576,197 Pachón cavefish-specific reads and 438,978 surface fish-specific reads. Using this dataset, we assembled transcriptomes of cave and surface fish separately, as well as an integrated transcriptome that combined 1,499,568 reads from both morphotypes. The integrated assembly was the most successful approach, yielding 22,596 high quality contiguous sequences comprising a total transcriptome length of 21,363,556 bp. Sequence identities were obtained through exhaustive blast searches, revealing an adult transcriptome represented by highly diverse Gene Ontology (GO) terms. Our dataset facilitated rapid identification of sequence polymorphisms between morphotypes. These data, along with positional information collected from the Danio rerio genome, revealed several syntenic regions between Astyanax and Danio. We demonstrated the utility of this positional information through a QTL analysis of albinism in a surface x Pachón cave F(2) pedigree, using 65 polymorphic markers identified from our integrated assembly. We also adapted our dataset for an RNA-seq study, revealing many genes responsible for visual system maintenance in surface fish, whose expression was not detected in adult Pachón cavefish. Conversely, several metabolism-related genes expressed in cavefish were not detected in surface fish. This resource will enable powerful genetic and genomic analyses in the future that will better clarify the heritable genetic changes governing adaptation to the cave environment.

Project description:BackgroundCave animals converge evolutionarily on a suite of troglomorphic traits, the best known of which are eyelessness and depigmentation. We studied 11 cave and 10 surface populations of Astyanax mexicanus in order to better understand the evolutionary origins of the cave forms, the basic genetic structuring of both cave and surface populations, and the degree to which present day migration among them affects their genetic divergence.ResultsTo assess the genetic structure within populations and the relationships among them we genotyped individuals at 26 microsatellite loci. We found that surface populations are similar to one another, despite their relatively large geographic separation, whereas the cave populations are better differentiated. The cave populations we studied span the full range of the cave forms in three separate geographic regions and have at least five separate evolutionary origins. Cave populations had lower genetic diversity than surface populations, correlated with their smaller effective population sizes, probably the result of food and space limitations. Some of the cave populations receive migrants from the surface and exchange migrants with one another, especially when geographically close. This admixture results in significant heterozygote deficiencies at numerous loci due to Wahlund effects. Cave populations receiving migrants from the surface contain small numbers of individuals that are intermediate in both phenotype and genotype, affirming at least limited gene flow from the surface.ConclusionsCave populations of this species are derived from two different surface stocks denoted "old" and "new." The old stock colonized caves at least three times independently while the new stock colonized caves at least twice independently. Thus, the similar cave phenotypes found in these caves are the result of repeated convergences. These phenotypic convergences have occurred in spite of gene flow from surface populations suggesting either strong natural or sexual selection for alleles responsible for the cave phenotype in the cave environment.

Dataset Information

Regressive evolution in the Mexican cave tetra, Astyanax mexicanus.

Publications

Regressive evolution in the Mexican cave tetra, Astyanax mexicanus.

Similar Datasets

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