The Rediscovery of a Long Described Species Reveals Additional Complexity in Speciation Patterns of Poeciliid Fishes in Sulfide Springs

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.

Speciation in Freshwater Fishes

“…Well-studied cases are those in livebearers of the genera Poecilia and Gambusia inhabiting sulfidic versus freshwater streams and caves in Mexico and the Caribbean. Multiple cases of early and advanced incipient speciation and some cases of older speciation events, both parapatric and allopatric, have been demonstrated in both genera (Palacios et al 2013, Riesch et al 2014, associated with strong but asymmetric divergent selection between and adaptation to sulfidic and hypoxic waters versus normoxic freshwaters.…”

Patterns of Macroinvertebrate and Fish Diversity in Freshwater Sulphide Springs

“…Most phenotypic traits investigated show strong signals of convergent evolution in evolutionarily independent lineages of Poecilia as well as other poeciliid taxa investigated to date [71,74,76,77].…”

“…Indeed, ecological speciation theory posits that reproductive isolation between populations can emerge incidentally as a by-product of adaptive trait divergence [135,136], and multifarious selection generated by the complex environmental differences between adjacent sulphidic and non-sulphidic environments may further promote the speciation process [137]. The majority of sulphide spring Poecilia and Gambusia are genetically differentiated from adjacent, ancestral populations in non-sulphidic environments, despite small geographic distances (in some instances <100 meters) and a lack of physical barriers that could prevent fish migration [70,77,138]. In the genus Poecilia, reproductive isolation is at least in part mediated by selection against immigrants.…”

“…In Southern Mexico, sulphide springs occur in a replicated fashion in the states of Tabasco and Chiapas, particularly in the region around the city of Teapa [76,77]. Here, the mountains of the Sierra Madre de Chiapas meet the wide floodplains of northern Tabasco, and sulphide springs can be found in four major tributaries of the Rio Grijalva: the Rios Tacotalpa, Puyacatengo, Ixtapangajoya, and Pichucalco (from east to west; Figure 3).…”

“…This is highlighted in the different number of species occurring at adjacent sites that differ in the presence or absence of H 2 S, but are separated by <100 m (e.g., the different branches of the Rio El Azufre in the Pichucalco drainage, and La Lluvia big spring and the upstream site of Arroyo La Lluvia in the Puyacatengo drainage). Species of the genus Poecilia were collected in all sulphide springs investigated; nominally, this included sulphidic ecotypes of Poecilia mexicana in the springs of the Tacotalpa and Puyacatengo drainages, P. thermalis in the Ixtapangajoya (endemic to the two La Esperanza springs), and P. sulphuraria in the Pichucalco (endemic to the Baños del Azufre and its outflows, as well as the La Gloria springs; see [77] for a discussion of the convoluted taxonomy of this group). Sulphidic ecotypes in all drainages are reproductively isolated, genetically differentiated, and differ from conspecifics from adjacent non-sulphidic habitats in a series of phenotypic traits, including physiological, morphological, behavioural, and life history characteristics (see Sections 3.2.2. and 3.2.3.…”