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      Phylogeographical convergence between Astyanax cavefish and mysid shrimps in the Sierra de El Abra, Mexico

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      Subterranean Biology
      Pensoft Publishers

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          Abstract

          The Sierra de El Abra is a long (120 km) and narrow (10 km) karstic area in northeastern Mexico. Some studies have suggested independent evolutionary histories for the multiple populations of blind cavefish Astyanax mexicanus that inhabit this mountain range, despite the hydrological connections that may exist across the Sierra. Barriers between caves could have prevented stygobitic populations to migrate across caves, creating evolutionary significant units localized in discrete biogeographical areas of the Sierra de El Abra. The goal of the present study was to evaluate if there is a correspondence in phylogeographical patterns between Astyanax cavefish and the stygobitic mysid shrimp Spelaeomysis quinterensis. Astyanax mtDNA and mysid histone H3 DNA sequences showed that in both species, cave populations in central El Abra, such as Tinaja cave, are broadly different from other cave populations. This phylogeographical convergence supports the notion that the central Sierra de El Abra is a biogeographical zone with effective barriers for either cave to cave or surface to cave gene flow, which have modulated the evolutionary history across species of its aquatic stygobitic community.

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          The complex origin of Astyanax cavefish

          Background The loss of phenotypic characters is a common feature of evolution. Cave organisms provide excellent models for investigating the underlying patterns and processes governing the evolutionary loss of phenotypic traits. The blind Mexican cavefish, Astyanax mexicanus, represents a particularly strong model for both developmental and genetic analyses as these fish can be raised in the laboratory and hybridized with conspecific surface form counterparts to produce large F2 pedigrees. As studies have begun to illuminate the genetic bases for trait evolution in these cavefish, it has become increasingly important to understand these phenotypic changes within the context of cavefish origins. Understanding these origins is a challenge. For instance, widespread convergence on similar features renders morphological characters less informative. In addition, current and past gene flow between surface and cave forms have complicated the delineation of particular cave populations. Results Past population-level analyses have sought to: 1) estimate at what time in the geological past cave forms became isolated from surface-dwelling ancestors, 2) define the extent to which cave form populations originated from a common invasion (single origin hypothesis) or several invasions (multiple origin hypothesis), and 3) clarify the role of geological and climatic events in Astyanax cavefish evolution. In recent years, thanks to the combined use of morphological and genetic data, a much clearer picture has emerged regarding the origins of Astyanax cavefish. Conclusions The consensus view, based on several recent studies, is that cave forms originated from at least two distinct ancestral surface-dwelling stocks over the past several million years. In addition, each stock gave rise to multiple invasions of the subterranean biotope. The older stock is believed to have invaded the El Abra caves at least three times while the new stock separately invaded the northern Guatemala and western Micos caves. This renewed picture of Astyanax cavefish origins will help investigators draw conclusions regarding the evolution of phenotypic traits through parallelism versus convergence. Additionally, it will help us understand how the presence of cave-associated traits in old versus young cave populations may be influenced by the time since isolation in the cave environment. This will, in turn, help to inform our broader understanding of the forces that govern the evolution of phenotypic loss.
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            Evolutionary history of the fish genus Astyanax Baird & Girard (1854) (Actinopterygii, Characidae) in Mesoamerica reveals multiple morphological homoplasies

            Background Mesoamerica is one of the world's most complex biogeographical regions, mostly due to its complex geological history. This complexity has led to interesting biogeographical processes that have resulted in the current diversity and distribution of fauna in the region. The fish genus Astyanax represents a useful model to assess biogeographical hypotheses due to it being one of the most diverse and widely distributed freshwater fish species in the New World. We used mitochondrial and nuclear DNA to evaluate phylogenetic relationships within the genus in Mesoamerica, and to develop historical biogeographical hypotheses to explain its current distribution. Results Analysis of the entire mitochondrial cytochrome b (Cytb) gene in 208 individuals from 147 localities and of a subset of individuals for three mitochondrial genes (Cytb, 16 S, and COI) and a single nuclear gene (RAG1) yielded similar topologies, recovering six major groups with significant phylogeographic structure. Populations from North America and Upper Central America formed a monophyletic group, while Middle Central America showed evidence of rapid radiation with incompletely resolved relationships. Lower Central America lineages showed a fragmented structure, with geographically restricted taxa showing high levels of molecular divergence. All Bramocharax samples grouped with their sympatric Astyanax lineages (in some cases even with allopatric Astyanax populations), with less than 1% divergence between them. These results suggest a homoplasic nature to the trophic specializations associated with Bramocharax ecomorphs, which seem to have arisen independently in different Astyanax lineages. We observed higher taxonomic diversity compared to previous phylogenetic studies of the Astyanax genus. Colonization of Mesoamerica by Astyanax before the final closure of the Isthmus of Panama (3.3 Mya) explains the deep level of divergence detected in Lower Central America. The colonization of Upper Mesoamerica apparently occurred by two independent routes, with lineage turnover over a large part of the region. Conclusion Our results support multiple, independent origins of morphological traits in Astyanax, whereby the morphotype associated with Bramocharax represents a recurrent trophic adaptation. Molecular clock estimates indicate that Astyanax was present in Mesoamerica during the Miocene (~8 Mya), which implies the existence of an incipient land-bridge connecting South America and Central America before the final closure of the Isthmus of Panama (~3.3 Mya).
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              Evidence for multiple genetic forms with similar eyeless phenotypes in the blind cavefish, Astyanax mexicanus.

              A diverse group of animals has adapted to caves and lost their eyes and pigmentation, but little is known about how these animals and their striking phenotypes have evolved. The teleost Astyanax mexicanus consists of an eyed epigean form (surface fish) and at least 29 different populations of eyeless hypogean forms (cavefish). Current alternative hypotheses suggest that adaptation to cave environments may have occurred either once or multiple times during the evolutionary history of this species. If the latter is true, the unique phenotypes of different cave-dwelling populations may result from convergence of form, and different genetic changes and developmental processes may have similar morphological consequences. Here we report an analysis of variation in the mitochondrial NADH dehydrogenase 2 (ND2) gene among different surface fish and cavefish populations. The results identify a minimum of two genetically distinctive cavefish lineages with similar eyeless phenotypes. The distinction between these divergent forms is supported by differences in the number of rib-bearing thoracic vertebrae in their axial skeletons. The geographic distribution of ND2 haplotypes is consistent with roles for multiple founder events and introgressive hybridization in the evolution of cave-related phenotypes. The existence of multiple genetic lineages makes A. mexicanus an excellent model to study convergence and the genes and developmental pathways involved in the evolution of the eye and pigment degeneration.
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                Author and article information

                Journal
                Subterranean Biology
                SB
                Pensoft Publishers
                1314-2615
                1768-1448
                August 14 2018
                August 14 2018
                : 26
                : 75-84
                Article
                10.3897/subtbiol.26.27097
                0be39ba6-1351-4cbc-851c-95301ead153d
                © 2018

                http://creativecommons.org/licenses/by/4.0/

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