Abstract
The process of ecological speciation drives the evolution of locally adapted and reproductively isolated populations in response to divergent natural selection. In Southern Mexico, several lineages of the freshwater fish species of the genus Poecilia have independently colonized toxic, hydrogen sulfide-rich springs. Even though ecological speciation processes are increasingly well understood in this system, aligning the taxonomy of these fish with evolutionary processes has lagged behind. While some sulfide spring populations are classified as ecotypes of Poecilia mexicana, others, like P. sulphuraria, have been described as highly endemic species. Our study particularly focused on elucidating the taxonomy of the long described sulfide spring endemic, Poecilia thermalis Steindachner 1863, and investigates if similar evolutionary patterns of phenotypic trait divergence and reproductive isolation are present as observed in other sulfidic species of Poecilia. We applied a geometric morphometric approach to assess body shape similarity to other sulfidic and non-sulfidic fish of the genus Poecilia. We also conducted phylogenetic and population genetic analyses to establish the phylogenetic relationships of P. thermalis and used a population genetic approach to determine levels of gene flow among Poecilia from sulfidic and non-sulfidic sites. Our results indicate that P. thermalis' body shape has evolved in convergence with other sulfide spring populations in the genus. Phylogenetic analyses placed P. thermalis as most closely related to one population of P. sulphuraria, and population genetic analyses demonstrated that P. thermalis is genetically isolated from both P. mexicana ecotypes and P. sulphuraria. Based on these findings, we make taxonomic recommendations for P. thermalis. Overall, our study verifies the role of hydrogen sulfide as a main factor shaping convergent, phenotypic evolution and the emergence of reproductive isolation between Poecilia populations residing in adjacent sulfidic and non-sulfidic environments.
Highlights
Divergent natural selection, often mediated by environmental variation, is a key driver of phenotypic evolution
Inspection of divergence scores indicated that P. thermalis, just like Poecilia from the Tacotalpa and the Pichucalco drainages, exhibits a body shape typical for sulfide spring populations
Our results indicate that sulfide springs in the Pichucalco and the Ixtapangajoya drainages were not colonized independently, but rather P. sulphuraria and P. thermalis are of a single evolutionary origin despite their current distribution in independent drainages, which in the area of the sulfide springs are separated by mountainous terrain reaching more than 500 meters above the surrounding elevation
Summary
Often mediated by environmental variation, is a key driver of phenotypic evolution. Depending on the strength of selection and rates of gene flow, such local adaptation may cause the emergence of reproductive isolating barriers among diverging populations as a byproduct, a process known as ecological speciation [2,3,4]. Such speciation driven by adaptation has been documented in a variety of organisms and in response to a diversity of selective forces (e.g., resource exploitation [5,6], habitat use [7,8], and predation [9,10]). The fact that phenotypic divergence is not necessarily tied to the emergence of reproductive isolation, as well as the dynamic nature of species boundaries, pose a challenge for efforts in biological systematics and taxonomy, which attempt to describe and organize biological diversity [14]
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