A geographical cline in craniofacial morphology across populations of Mesoamerican lake‐dwelling fishes

Abstract

Together, the complex geological history and climatic diversity of Mesoamerica create a rich source of biodiversity from which evolutionary processes can be studied. Here, we discuss highly divergent morphs of lake‐dwelling fishes distributed across Mexico and Central America, originally recognized as members of different genera (Astyanax and “Bramocharax”). Recent phylogenetic studies, however, suggest these morphs group within the same genus and readily hybridize. Despite genetic similarities, Bramocharax morphs exhibit stark differences in cranial shape and dentition. We investigated the evolution of several cranial traits that vary across morphs collected from four lakes in Mexico and Nicaragua and discovered an ecomorphological cline from northern to southern lakes. Northern populations of sympatric morphs exhibit a similar cranial shape and tooth morphology. Southern populations of Bramocharax morphs, however, showed a larger disparity in maxillary teeth, length and frequency of unicuspid teeth, an elongated snout, and a streamlined cranium compared to Astyanax morphs. This divergence of craniofacial morphology likely evolved in association with differences in trophic niches. We discuss the morphological differences across the four lake systems in terms of geological history and trophic dynamics. In summary, our study suggests that Bramocharax morphs are likely locally adapted members derived from independent Astyanax lineages, highlighting an interesting parallel evolutionary pattern within the Astyanax genus.

Genetic and ecomorphological divergence between sympatricAstyanaxmorphs from Central America

“…The Astyanax found in Lake Catemaco may correspond to a younger lineage of the genus than that in the San Juan River basin (Ornelas-García et al, 2008), which could represent an older diverging lineage with discrete levels of genetic differentiation. Congruent with this genetic divergence, Garita-Alvarado et al (2018) and Powers et al (2020) found a higher level of morphological divergence between morphs in the San Juan River system than between those from Lake Catemaco. Additionally, besides time, Nosil et al (2009) noted other factors that could influence the ecological speciation process including the nature of the divergent selection itself (e.g., strong vs. weak selection, or selection on a single trait vs. selection on a larger number of traits) and genetic factors (e.g., no physical linkage between genes under selection and those conferring reproductive isolation).…”

“…Despite the divergence in trophic-related traits (Garita-Alvarado et al, 2018;Powers et al, 2020) and the potential differences in trophic habits (Bussing, 1993), very few studies have characterized the level of genetic differentiation between the two morphs. Ornelas-García, Domínguez-Domínguez, & Doadrio (2008) showed that morphs have a close genetic relationship, and even share mitochondrial haplotypes.…”

Incipient genetic divergence or cryptic speciation? Procamallanus (Nematoda) in freshwater fishes (Astyanax)

“…Genetic evidence suggests that at least in one cave (Chica), an admixture occurs between individuals of A. mexicanus from surface and cave waters (Bradic et al, 2012; Strecker, Hausdorf & Wilkens, 2012; Herman et al, 2018). Another conspicuous example of parallel evolution under ecologically divergent scenarios within the genus is shown by the sympatric lacustrine species across Mexican and Central America tropical lakes, that is A. aeneus and A. caballeroi ; A. nasatus, A. nicaraguensis and A. bransfordii (Ornelas‐García et al, 2008; Powers et al, 2020). In Lake Catemaco, Mexico, the morphs of A. aeneus and A. caballeroi are highly divergent, and as a result, they were originally considered as different genera ( Astyanax and ‘ Bramocharax’ ); however, recent molecular studies have shown that they belong not only to the same genus, but also they readily hybridize and show no sign of genetic differentiation, although morphological and ecological differences are evident among Astyanax ecomorphs (Ornelas‐García et al, 2018).…”

Parallel Evolution of Allometric Trajectories of Trophic Morphology between Sympatric Morphs of Mesoamerican Astyanax (Characidae)

“…These fishes are known to adapt to a very wide range of ecological conditions, the cave-adapted morphs being the most conspicuous example [14][15][16][17]. Interestingly, previous works have found evidence of the parallel evolution of sympatric morphs associated with trophic morphology and body shape divergence in different Mesoamerican lakes inhabited by lineages of Astyanax, which evolved independently [18][19][20][21][22]. This has been shown in two distant geographical systems, the San Juan River basin in Central America (which includes the Lakes Managua and Nicaragua), and the Lake Catemaco system in Mexico [20,23,24].…”

“…The lacustrine morphs, consisting of an elongate-body and a deep-body morph (Figure 1), show major morphological differences, which prompted their original consideration as different genera (i.e., Astyanax and Bramocharax, [25,26]). Some of the morphological differences distinguishing these morphs correspond to the body depth and the head length, as well as to their trophic morphology (i.e., number of maxillary teeth and of cuspids on the anterior tooth of premaxilla, see [21,22]), which are associated with alternative trophic habits. Additionally, a geographical cline (i.e., a differentiation gradient between north and south systems) in morphological differentiation between morphs was suggested between the Lake Catemaco and San Juan River systems [22], and, recently, we explored the genetic and ecological differentiation between sympatric morphs of Astyanax in these systems, finding evidence of a geographical cline also in the genetic differentiation [23,24].…”