Primer to the basin and its biota (skip to second paragraph and beyond to see my past and present research in the basin)
I have been working in Cuatro Ciénegas since 1998. It is, without question, one of the more remarkable natural systems on Earth. The valley is nestled within the basin and range of the Chihuahuan Desert in Coahuila, Mexico. At about 200 square kilometers, Cuatro Ciénegas hosts a multitude of springs, rios, lagunas, and marshes. These variously connected aquatic habitats form gradient systems, spanning from physicochemically benign headsprings to environmentally severe marshes and terminal, evaporative lagunas. Within this diverse environmental setting is found one of the more concentrated assemblages of endemic aquatic species known to science. Along the transitions from physicochemically constant thermal springs, through intermediate habitats, and into environmentally severe, terminal lagunas and marshes, species diversity declines rapidly. Among the most well studied aquatic species are the highly diverse and largely endemic hydrobiid snail fauna and a phylogenetically rich assortment of fishes, of which 9 out of 16 native species are also endemic. Not only is the basin remarkable for its endemism but also the eclectic ancestral connections of the species that evolved here. For example, although a majority of endemic and native species are ancestrally associated with the Rio Grande (Rio Bravo) to the north, the pupfish Cyprinodon atrorus (top picture) has closest relatives to the west in the State of Durango (Rio Aguanaval and Rio Nazas); the Poeciliid Xiphophorus gordoni is the northernmost species of the genus, with closest relations to species in the Panuco basin to the south; and the mysterious C. bifasciatus (middle picture), which is ecologically and behaviorally atypical of the genus and is of uncertain biogeographic origin and phylogenetic placement within the genus; this species, however, is thought to represent one of the older endemic fish lineages in the basin and is likely a basal Cyprinodon. Thus, with respect to the aquatic fauna, the basin is rich in biodiversity from the perspectives of endemism, biogeographic origins, and diverse adaptations across a range of environmental conditions. Geologically, the basin is a wonder; hydrologically it for all practical purposes remains a mystery.
W. L. Minckley (Minck) on right, with Pepe Lugo, namesake of the endemic Tufa Darter (Etheostoma lugoi). Photo taken in the 1960s at the source-spring of Rio Puente Chiquita.
Research in the Cuatro Cienegas basin
My primary research focus has been on the two endemic pupfishes, C. atrous and C. bifasciatus, but I have recently been able to reach a long-term goal by getting to work on the microendemic Cuatro Ciénegas Platyfish Xiphophorus gordoni (Carson et al. in press)
Cuatro Ciénegas pupfishes
Of the two endemic pupfishes of Cuatro Ciénegas, C. atrous largely prefers severe, highly variable environments that support a depauperate piscine fauna, whereas C. bifasciatus is associated most closely with a diverse fish fauna within thermal headsprings and their environmentally buffered outflows. My research has focused on four areas: phylogeography within the basin (Carson and Dowling 2006), experimental evaluation of the phyicochemical tolerances of the two pupfishes (Carson et al. 2008), natural hybridization between these species (Carson et al. 2012), and relationships between environmental variation, hybridization, and phenotypic diversity (Tobler and Carson 2010). Most of my work has utilized mtDNA sequencing and assessment of nuclear intron variation across the entire geographic range of both taxa and within hybrid zones between them.
1) Phylogeography, hydrogeography, and historical introgressive hybridization
The Cuatro Ciénegas basin is divided roughly in half by a south to north trending, plunging anticline (Sierra San Marcos). Along the base of this mountain, a series of springs and rivers emerge. My initial investigations in the basin focused on characterizing mtDNA and nuclear DNA (intron and coding) sequence variation across the range of the two pupfishes, with an emphasis on understanding hydrogeographic history of the basin and the history of hybridization between these species. Essentially, mtDNA variation is geographically rather than taxonomically partitioned. A phylogeny of the genus (Echelle et al., 2005) and phylogeographic study of populations throughout the basin (Carson and Dowling 2006) confirmed that ancient hybridization between these species led to the complete, range-wide replacement of the mitochondrial genome of C. bifasciatus by that of C. atrorus. In contrast, nuclear DNA loci studied to date (CK-A, RAG-1 and TPI-B) between the species are essentially diagnostic but show little variation within the species, almost certainly due to choice of marker (i.e., nuclear introns and coding regions evolve more slowly that markers such as microsatellite loci); the use of nuclear DNA sequences was essential for study of hybridization dynamics.
2.) Physicochemical tolerance differences between C. atrorus and C. bifasciatus
Anecdotal evidence long suggested that, despite extensive hybridization, C. atrorus and C. bifasciatus are separated by significant differences in their physicochemical tolerances. Cyprinodon atrorus lives in highly variable and harsh environments, such as terminal marshes and evapoartive lagunas; whereas C. bifasciatus lives primarily in physicochemically constant thermal springs and physicochemically buffered outflows of source springs. Cyprindodon bifasciatus is thought to expand its range downstream in spring and summer, as conditions in these areas acquire a more spring-like profile, but contact its range in winter when downstream conditions become to cold. Whether there are differences in physicochemical tolerance among hybrid genotypes was the inspiration of reciprocal transplant experiments with the parental species.
Reciprocal transplant experiments with C. atrorus and C. bifasciatus (Carson et al. 2008) demonstrated that C. bifasciatus is highly sensitive to both cold conditions and highly variable temperatures (winter and sumer) and/or salinities (summer). Significant physicochemical tolerance differences possibly explain, in part, why these species remain distinct despite extensive hybridization. However, C. atrorus experienced 100% survival in C. bifasciatus habitat (winter and summer) when predators and other fishes were excluded, which suggests predation and/or competition prevents C. atrorus from successfully inhabiting the most environmentally benign habitats, which are instead dominated by C. bifasciatus. The next point (3) demonstrates that the genetic basis of these adaptational differences is also likely to influence seasonal changes in the distribution and abundance of different types of hybrid genotypes.
3.) Spatio-temporal hybridization dynamics between C. atrorus andC. bifasciatus
Spatio-temporal monitoring of genetic (nuclear DNA loci) and environmental variation (salinity and temperature) was conducted over winter, spring, and summer for three consecutive years in the Rio Churince system. This study explicitly tested 1) whether there is spatial and temporal variation in environmental and genetic characteristics of pupfish within the Rio Churince hybrid zone; 2) how environmental variation is related to the genetic composition of Cyprinodon across sites in the hybrid zone; and 3) if there are season changes in the genetic composition of hybrids across the entire system. Results from this study demonstrated that spatio-temporal variation in the genetic composition (genotypic differences) of hybrids is predictable and driven by seasonal changes in environmental variation, as measured by changes in specific conductance and temperature (Carson et al. 2012). This study provides further evidence in support of an increasingly compelling argument that exogenous selection can be important in the regulation of hybrid zone dynamics; this, consequently, supports growing evidence that introgressive hybridization has been of evolutionary importance in animals.
4.) Relationships between hybridization, environmental variation, and phenotypic diversification of Cuatro Cienegas Cyprinodon.
A basin-wide analysis of environmental, genetic, and morphological variation was used to test hypotheses of tdriving influences on the phenotypic diversification of Cuatro Ciénegas Cyprinodon (Tobler and Carson 2010). Results indicate that not only has introgressive hybridization been important to the morphological diversity within pupfish in this basin, but that transgressive segregation (morphological characteristics that lie outside the range of parental species and extend beyond the intermediate morphospace between them) might also have had a crucial influence on phenotypic diversity. Environmental variation among sites has clearly been important, and interaction between these influences is likely. The relative roles of local adaptation and phenotypic plasticity await upcoming plans to experimentally test differences in physiological performance and biotic interactions (predation susceptibility) among C. atrorus, C. bifasciatus, and various hybrids and introgressed populations. This study revealed important information on the long-term evolutionary importance of introgressive hybridization in the morphological diversification of Cuatro Ciénegas pupfishes. Results from this study and Carson et al 2012 (Number 3, above) provide a crucial link between the importance of exogenous selection in contemporary hybrid zones and the influence of introgressive hybridization in the phenotypic diversification of Cuatro Ciénegas pupfishes. Critically, this connection is demonstrated, within the same system.