Environmental variation,hybridization, and phenotypic diversification in Cuatro Ciénegas pupfishes

Hybridization can generate novel phenotypes, and in combination with divergent selection along environmental gradients, can play a driving role in phenotypic diversification. This study examined the influence of introgressive hybridization and environmental variation on the phenotypic diversity of two pupfish species (Cyprinodon atrorus and Cyprinodon bifasciatus) endemic to the Cuatro Ciénegas basin, Mexico. These species occupy opposite environmental extremes and are comprised of multiple, intraspecifically isolated populations. However, interspecific hybridization occurs to various degrees within connecting, intermediate environments. Using geometric morphometric analysis, extensive variation of body shape was observed between and within species, and phenotypic variation was strongly correlated with environmental conditions. Furthermore, some introgressed populations exhibited unique phenotypes not found in either of the parents, and overall morphospace occupation was significantly higher in introgressed populations when compared to the parentals. Overall, we find environmental variation and transgressive segregation both appear to have been important in shaping phenotypic variation in this system.     

Role of Fish in Structuring Invertebrates on Stromatolites in Cuatro Ciénegas, México

Stromatolites, the dominant Precambrian life form, declined in the Phanerozoic to occur today in only a few sites. This decline has been attributed to evolution of metazoan grazers, but stromatolites in our study site, Cuatro Ciénegas, Coahuila, México, harbor diverse macroinvertebrates. Drawing on food chain theory, we hypothesized that fish predation on invertebrates controls invertebrate populations, allowing stromatolites to flourish in Cuatro Ciénegas. Our experiment used small mesh (1 mm) cages to exclude all but larval fishes, and larger (6.5 mm) cages to exclude all larger fishes (including the molluscivorous and omnivorous endemic polymorphic cichlid, Herichthys minckleyi), but allow access to all sizes of the abundant endemic pupfish, Cyprinodon bifasciatus. No effects of treatments on invertebrate densities were noted at 6 week, but significant effects were observed on specific taxonomic groups after 3 month. In absence of fishes, hydrobiidae snails and ceratopogonids increased 3- and 5-fold, respectively, and invertebrate assemblage composition varied among treatments. Algal biomass was not affected by treatments, but algal species composition appeared to change. Overall results suggest that fish assemblages structure invertebrate assemblages, and that fishes may also be factors in determining algal communities.     

Relationship between soil P fractions and microbial biomass in an oligotrophic grassland-desert scrub system

Phosphorus (P) is an essential element of the biosphere, both as a constituent of living organisms and as a regulator of biological processes. The Cuatro Ciénegas Basin in the central Chihuahuan Desert of Mexico is characterized by extreme P oligotrophy. The aim of this study was to quantify P distribution in soil P fractions, P sorption capacity, and P in microbial biomass in a desert scrub and grassland soil system in the Churince area of the Cuatro Ciénegas Basin over summer and winter seasons. Our objective, as part of an exploration of ecosystem functioning, was to ascertain the relationship between soil P fractions and P in microbial biomass. Our results demonstrate a scarcity of P, mainly in grassland, and also a higher P sorption capacity in grassland soil than in desert scrub. Desert scrub soil retained more P (228 ± 5 μg g^?1 dry soil) than grassland soil (87 ± 10 μg g^?1 dry soil), mainly in inorganic forms, but grassland soil retained more P in accessible organic forms. We suggest that biotic controls regulated by access to water shape the dynamics of soil P availability in the Churince grassland-desert scrub system.     

Sound Production in Cyprinodon bifasciatus (Cyprinodontiformes)

Sound production in Cyprinodon bifasciatus, a pupfish endemic to the Cuatro Ciénegas basin, Coahuila, México, is documented. The average dominant frequency is 409Hz, with an average duration of 55msec. Calls were produced by males during pursuits of conspecifics and cichlids, during territory patrol, while following a female and after spawning. There are differences in call structure between contexts, especially postspawn calls versus pursuit and courtship calls. There may be differences between sites, especially Mojarral Oeste versus Becerra and Churince. Given sound production in this species of Cyprinodon and the related genus Fundulus, it is possible that sound production is more widespread than previously thought in Atherinimorpha. In addition, this is another documentation of sound production in a clear freshwater species indicating that sound production is widespread in clear freshwater fish.     

Phylogeography, genetic structure, and gene flow in the endemic freshwater shrimp Palaemonetes suttkusi from Cuatro Ci��negas, Mexico

The valley of Cuatro Ciénegas in Mexico has the highest degree of local endemicity of any habitat in North America. A large number of endemic aquatic species occur both in the Cuatro Ciénegas basin and in the upper parts of the Río Salado de los Nadadores drainage, located immediately to the east of the valley. No natural surface flow occurs between these basins but artificial canals connect both areas. It is not clear whether the sharing of endemics between the Cuatro Ciénegas basin and the Río Salado is due to migration through canals. We conducted a phylogeographic study of mitochondrial haplotypes of the endemic shrimp Palaemonetes suttkusi to determine the evolutionary distinctiveness of the population found in Río Salado. We discovered that P. suttkusi likely has occurred naturally in both basins well into the distant past. Based on molecular clock analyses of the COI gene, the populations in the Río Salado and much of the Cuatro Ciénegas basin likely began diverging from each other between 1.9 and 11.2 Myr ago. The general levels of divergence are substantial but our results suggest there has also likely been recent gene flow between these basins. This is consistent with migration through human-made canals, but also consistent with the occurrence of natural gene flow during intermittent wet periods in the past million years. We also found significant differentiation of the Pozas Azules area from the rest of the Cuatro Ciénegas basin, a finding that is concordant with several phylogeographic studies on other aquatic endemics in Cuatro Ciénegas. We recommend that the upper parts of the Río Salado, the Pozas Azules area, and the rest of the Cuatro Ciénegas basin should each be considered independent evolutionarily significant units for conservation, and that migration of species through human-made canals should be monitored and controlled.     

Two Pseudomonas aeruginosa clonal groups belonging to the PA14 clade are indigenous to the Churince system in Cuatro Ciénegas Coahuila,México

Pseudomonas aeruginosa is a widely distributed environmental bacterium but is also an opportunistic pathogen that represents an important health hazard due to its high intrinsic antibiotic resistance and its production of virulence factors. The genetic structure of P. aeruginosa populations using whole genome sequences shows the existence of three clades, one of which (PA7 clade) has a higher genetic diversity. These three clades include clinical and environmental isolates that are very diverse in terms of geographical origins and isolation date. Here, we report the characterization of two distinct clonal P. aeruginosa groups that form a part of the PA14 clade (clade 2) sampled from the Churince system in Cuatro Ciénegas Basin (CCB). One of the clonal groups that we report here was isolated in 2011 (group 2A) and was displaced by the other clonal group (2B) in 2015. Both Churince groups are unable to produce pyoverdine but can produce other virulence-associated traits. The existence of these unique P. aeruginosa clonal groups in the Churince system is of ecological and evolutionary significance since the microbiota of this site is generally very distinct from other lineages, and this is the first time that a population of P. aeruginosa has been found in CCB.     

THE ROLE OF DIATOMS IN STROMATOLITE GROWTH: TWO EXAMPLES FORM MODERN FRESHWATER SETTINGS1

Some modern laminated find calcified stromatolitic structures are partially or completely formed by eukaryotes. Diatom populations in freshwater environments with elevated ionic concentrations contribute to calcite precipitation, and the formation of distinctive mineral-rich stromatolitic laminae. Two types of stromatolite-forming diatom populations were observed. In the first example, in stromatolites growing on a quarry ledge near Laegerdorf, North Germany, calcite crystals with biogenic imprints form around polysaccharide stalks of the diatom Gomphonema olivaceum var. calcarea (Cleve) Cleve-Euler. These individually precipitated crystals eventually become cemented together in layers, forming rigid, laminated stromatolitic deposits which drape over the quarry ledge. In the second example, in stromatolites forming in a shallow stream near Cuatro Ciénegas, Coahuila, Mexico, diatomaceous laminae also form by the accumulation of carbonate particles in a matrix of diatoms and their extracellular polysaccharide products. These laminae become thick enough to drape over individual stromatolite heads. The diatoms responsible for these deposits are Amphora aff. A. katii Selva, Nitzschia denticula Grun., and six other species. At Cuatro Ciénegas, in addition to the diatomaceous laminae, carbonate-rich cyanobacterial layers, dominated by two cyanobacterial species with different fabrics and porosities, are also present and contribute substantially to the growth of the stromatolites. In both the Laegerdorf and Cuatro Ciénegas examples, entire stromatolites or thick laminations on stromatolites are built by a small number of diatom species which produce copious amounts of extracellular stalk, gel, and sheath material, a propertuy they share with cyanobacterial stromatolite builders.     

MACHAERANTHERA RESTIFORMIS (ASTERACEAE) A BIZARRE NEW GYPSOPHILE FROM NORTHCENTRAL MEXICO

A rayless, diploid (n = 4), shrubby, new species of Machaeranthera is described from gypsum dunes near Cuatro Ciénegas, Coahuila. It is most closely related to M. johnstonii, another rayless, shrubby, endemic gypsophile of this region. Machaeranthera restiformis often occurs with the wide-ranging, white-rayed species, M. gypsophila (n = 4) with which it occasionally hybridizes.     

A new species of Mimosa (Leguminosae) from Coahuila,Mexico

Mimosaunipinnata from the Sierra de San Marcos in the Cuatro Ciénegas Basin of central Coahuila, Mexico, is described. It is unique among mimosas in having oncepinnate leaves.     

Diversity of culturable thermo-resistant aquatic bacteria along an environmental gradient in Cuatro Ciénegas,Coahuila, México

At the desert oasis of Cuatro Ciénegas in Coahuila, México, more than 300 oligotrophic pools can be found and a large number of endemic species of plants and animals. The most divergent taxa of diatoms, snail and fishes are located in the Churince hydrological system, where we analyzed the local diversification of cultivable Firmicutes and Actinobacteria. The Churince hydrological system is surrounded by gypsum dunes and has a strong gradient for salinity, temperature, pH and dissolved oxygen. In August 2003, surface water samples were taken in 10 sites along the Churince system together with the respective environmental measurements. 417 thermo-resistant bacteria were isolated and DNA was extracted to obtain their BOX-PCR fingerprints, revealing 55 different patterns. In order to identify similarities and differences in the diversity of the various sampling sites, an Ordination Analysis was applied using Principal Component Analysis. This analysis showed that conductivity is the environmental factor that explains the distribution of most of the microbial diversity. Phylogenetic reconstruction from their 16S rRNA sequences was performed for a sample of 150 isolates. Only 17 sequences had a 100% match in the Gene Bank (NCBI), representing 10 well known cosmopolitan taxa. The rest of the sequences cluster in 22 clades for Firmicutes and another 22 clades for Actinobacteria, supporting the idea of high diversity and differentiation for this site.     

First draft genome sequence of a strain from the genus Citricoccus

Bacteria of the genus Citricoccus have been isolated from ecological niches characterized by diverse abiotic stress conditions. Here we report the first genome draft of a strain of the genus Citricoccus isolated from the extremely oligotrophic Churince system in the Cuatro Ciénegas Basin (CCB) in Coahuila, Mexico.     

Involvement of cyclodipeptides in the competition of bacterial communities in the oligotrophic Churince aquatic system of Cuatro Ciénegas Basin dominated by Gammaproteobacteria

The Cuatro Ciénegas Basin (CCB) within the Chihuahuan Desert in México is an extremely oligotrophic oasis with negligible phosphorous levels, described as a hot spot of biodiversity, not only in stromatolites and microbial mats, but also in living forms in general. The microorganisms possess the capability to produce a wide variety of virulence factors, antibiotics, and quorum-sensing (QS) crosstalk signals such as non-ribosomal cyclodipeptides (CDPs) which enables them to colonize diverse ecological niches. In the aquatic system of CCB known as Churince, a bacterial population was isolated from the Lagunita pond dominated by Gammaproteobacteria. In this work, we determined the relationships between the antagonism and CDPs production in this bacterial population. Results indicate that 68% of isolates showed antagonistic effects over other isolates, correlating with production of CDPs and the antibiotic 2,4-diacetylphloroglucinol (DAPG). Although a minority of the isolates were capable of inducing a QS biosensor strain, bacterial QS interference was not the main mechanism in the antagonism observed. Thus, our results indicate that CDPs primarily, and DAPG to a lesser degree, are involved with the growth-inhibition competition mechanisms of bacterial communities in the Lagunita pond and was associated with a Gammaproteobacteria dominancy phenomena.

     

THE ROLE OF DIATOMS IN STROMATOLITE GROWTH: TWO EXAMPLES FROM MODERN FRESHWATER SETTINGS1

Some modern laminated and calcified stromatolitic structures are partially or completely formed by eukaryotes. Diatom populations in freshwater environments with elevated ionic concentrations contribute to calcite precipitation, and the formation of distinctive mineral-rich stromatolitic laminae. Two types of stromatolite-forming diatom populations were observed. In the first example, in stromatolies growing on a quarry ledge near Laegerdorf, North Germany, calcite crystals with biogenic imprints form around polysaccharide stalks of the diatom Gomphonema olivaceum var. calcarea (Cleve) Cleve-Euler. These individually precipitated crystals eventunally become cemented together in layers, forming rigid, laminated stromatolitic deposits which drape over the quarry ledge. In the second example, in stromatolites forming in a shallow stream near Cuatro Ciénegas, Coahuila, Mexico, diatomaceous laminae also form by the accumulation of carbonate particles in a matrix of diatoms and their extracellular polysaccharide products. These laminae become thick enough to drape over individual stromatolite heads. The diatoms responsible for these deposits are Amphora aff. A. Katii Selva, Nitzschia denticula Grun., and six other species. At Cuatro Ciénegas, in addition to the diatomaceous laminae, carbonate-rich cyanobacterial layers, dominated by two cyanobacterial species with different fabrics and porosities, are also present and contribute substantially to the growth of the stromatolites. In both the Laegerdorf and Cuatro Ciénegas examples, entire stromatolites or thick laminations on stromatolites are built by a small number of diatom species which produce copious amounts of extracellular stalk, gel, and sheath material, a property they share with cyanobacterial stromatolite builders.     

Predation drives morphological convergence in the Gambusia panuco species group among lotic and lentic habitats

Fish morphology is often constrained by a trade‐off between optimizing steady vs. unsteady swimming performance due to opposing effects of caudal peduncle size. Lotic environments tend to select for steady swimming performance, leading to smaller caudal peduncles, whereas predators tend to select for unsteady swimming performance, leading to larger caudal peduncles. However, it is unclear which aspect of performance should be optimized across heterogeneous flow and predation environments and how this heterogeneity may affect parallel phenotypic evolution. We investigated this question among four Gambusia species in north‐eastern Mexico, specifically the riverine G. panuco, the spring endemics G. alvarezi and G. hurtadoi, and a fourth species, G. marshi, found in a variety of habitats with varying predation pressure in the Cuatro Ciénegas Basin and Río Salado de Nadadores. We employed a geometric morphometric analysis to examine how body shapes of both male and female fish differ among species and habitats and with piscivore presence. We found that high‐predation and low‐predation species diverged morphologically, with G. marshi exhibiting a variable, intermediate body shape. Within G. marshi, body morphology converged in high‐predation environments regardless of flow velocity, and fish from high‐predation sites had larger relative caudal peduncle areas. However, we found that G. marshi from low‐predation environments diverged in morphology between sub‐basins of Cuatro Ciénegas, indicating other differences among these basins that merit further study. Our results suggest that a morphological trade‐off promotes parallel evolution of body shape in fishes colonizing high‐predation environments and that changing predation pressure can strongly impact morphological evolution in these species.     

Introgressive hybridization in a trophically polymorphic cichlid

Trophically polymorphic species could represent lineages that are rapidly diverging along an ecological axis or could phenotypically mark the collapse of species through introgressive hybridization. We investigated patterns of introgression between the trophically polymorphic cichlid fish Herichthys minckleyi and its relative H. cyanoguttatus using a combination of population genetics and species tree analyses. We first examined the distribution of mitochondrial haplotypes within the alternative H. minckleyi pharyngeal jaw morphotypes that are endemic to the small desert valley of Cuatro Ciénegas. We recovered two clusters of mitochondrial haplotypes. The first contained a number of slightly differentiated cytochrome b (cytb) haplotypes that showed some phylogeographic signal and were present in both jaw morphotypes. The other haplotype was monomorphic, highly differentiated from the other cluster, present in equal frequencies in the morphotypes, and identical to H. cyanoguttatus haplotypes found outside Cuatro Ciénegas. Then, we investigated whether H. minckleyi individuals with the H. cyanoguttatus cytb were more evolutionarily similar to H. cyanoguttatus or other H. minckleyi using a species tree analysis of 84 nuclear loci. Both H. minckleyi pharyngeal morphotypes, regardless of their cytb haplotype, were quite distinct from H. cyanoguttatus. However, hybridization could be blurring subdivision within H. minckleyi as the alternative jaw morphotypes were not genetically distinct from one another. Accounting for introgression from H. cyanoguttatus will be essential to understand the evolution of the trophically polymorphic cichlid H. minckleyi.     

Ecophysiology of first and second generation hybrids in a natural plant hybrid zone

Hybrids between related species vary widely in relative fitness, and that fitness can depend upon the environment. We investigated aspects of physiology that might influence fitness patterns in a plant hybrid zone. Seeds of Ipomopsis aggregata, I. tenuituba, F1 hybrids, F2 hybrids, and offspring of crosses between natural hybrids were planted into the relatively mesic site of origin for I. aggregata and the drier site for natural hybrids. We measured rates of photosynthesis (A _max), transpiration (E), instantaneous (A/E) and long-term (δ¹³C) indices of water use efficiency (WUE), and leaf nitrogen and carbon. We also examined correlations of these traits with plant size. Photosynthetic rate and A/E were higher in vegetative than flowering plants. WUE varied between sites and years, but differences among genotypic classes were spatially and temporally consistent. Instantaneous WUE was higher for F1 hybrids than for the average of the parental species, thereby showing heterosis. There was no evidence of hybrid breakdown, as WUE was no different in the F2 than the average across the F1 and parental species. Nor did WUE depend on cross direction in producing F1 progeny. Carbon isotope discrimination revealed higher long-term water use efficiency in I. tenuituba than I. aggregata. Leaf nitrogen was higher in I. tenuituba than I. aggregata, and higher in offspring of natural hybrids than in the F2. Results indicate heterosis for water use efficiency, with no hybrid breakdown. Heterosis in WUE may help to explain the relatively high survival of both reciprocal F1 hybrids in dry sites within the natural hybrid zone.     

Morphological variation of genetically confirmed Alouatta Pigra × A. palliata hybrids from a natural hybrid zone in Tabasco,Mexico

While hybridization has been reported for a large number of primate taxa, there is a general lack of data on hybrid morphology for wild individuals with known genetic ancestry. A confirmed hybrid zone for the closely related Neotropical primates Alouatta palliata and A. pigra has provided a unique opportunity to study primate hybrid morphological variation. Here we used molecular evidence based on mitochondrial, Y‐chromosome, and autosomal data to assess hybrid ancestry. We conducted univariate and multivariate statistical comparisons of morphometric data collected from individuals both outside and within the hybrid zone in Tabasco, Mexico. Our results show that of all the hybrids detected (N = 128), only 12% of them were approximately genetically intermediate, and none of them were first generation hybrids. Univariate pairwise comparisons among parental individuals, multigenerational backcrossed hybrids, and intermediate hybrids showed that overall, multigenerational backcrossed hybrids resemble the parental species with which they share most of their alleles. Conversely, intermediates were highly variable. Similarly, principal component analysis depicts an overlap between the parental species and their backcrosses when considering overall morphological differences. Finally, discriminant function analysis of the morphological variables was overall unreliable for classifying individuals into their assigned genotypic classes. Taken together, our results suggest that primate natural hybridization studies should incorporate molecular methods for determining ancestry, because morphology may not always be a reliable indicator of hybrid status. Hybrid zones could comprise a large number of multigenerational backcrossed hybrids that are indistinguishable from the parental species. The implications for studying hybridization in the primate fossil record are discussed. Am J Phys Anthropol, 2013. © 2012 Wiley Periodicals, Inc.     

NARROW HYBRID ZONE BETWEEN TWO SUBSPECIES OF BIG SAGEBRUSH (ARTEMISIA TRIDENTATA: ASTERACEAE). IV. RECIPROCAL TRANSPLANT EXPERIMENTS

Does endogenous or exogenous selection stabilize the big sagebrush (Artemisia tridentata) hybrid zone? After two years of study, our reciprocal transplant experiments showed significant genotype by environment interactions for a number of fitness components, including germination, growth, and reproduction. Hybrids were the most fit within the hybrid garden. In the parental gardens, the native parental taxon was more fit than either the alien parental or hybrids. These results are consistent with the bounded hybrid superiority model, which assumes exogenous selection, but are clearly at odds with the dynamic equilibrium model, which assumes endogenous selection and universal hybrid unfitness.     

Hybridization effects and genetic diversity of the common and black‐tufted marmoset (Callithrix jacchus and Callithrix penicillata) mitochondrial control region

Hybridization is continually documented in primates, but effects of natural and anthropogenic hybridization on biodiversity are still unclear and differentiating between these contexts remains challenging in regards to primate evolution and conservation. Here, we examine hybridization effects on the mitochondrial DNA (mtDNA) control region of Callithrix marmosets, which provide a unique glimpse into interspecific mating under distinct anthropogenic and natural conditions. DNA was sampled from 40 marmosets along a 50‐km transect from a previously uncharacterized hybrid zone in NE Brazil between the ranges of Callithrix jacchus and Callithrix penicillata. DNA was also collected from 46 marmosets along a 30‐km transect in a hybrid zone in Rio de Janeiro state, Brazil, where exotic marmosets appeared in the 1980s. Combining Callithrix DNA sampled inside and outside of these hybrid zones, phylogenetic and network analyses show C. jacchus and C. penicillata being parental species to sampled hybrids. We expand limited Callithrix population genetics work by describing mtDNA diversity and demographic history of these parental species. We show ancient population expansion in C. jacchus and historically constant population size in C. penicillata, with the latter being more genetically diverse than the former. The natural hybrid zone contained higher genetic diversity relative to the anthropogenic zone. While our data suggest hybrid swarm formation within the anthropogenic zone due to removed physical reproductive barriers, this pattern is not seen in the natural hybrid zone. These results suggest different genetic dynamics within natural and anthropogenic hybridization contexts that carry important implications for primate evolution and conservation. Am J Phys Anthropol 155:522–536, 2014. © 2014 Wiley Periodicals, Inc.     

Do relaxed selection and habitat temperature facilitate biased mitogenomic introgression in a narrowly endemic fish?

Introgression might be exceptionally common during the evolution of narrowly endemic species. For instance, in the springs of the small and isolated Cuatro Ciénegas Valley, the mitogenome of the cichlid fish Herichthys cyanoguttatus could be rapidly introgressing into populations of the trophically polymorphic H. minckleyi. We used a combination of genetic and environmental data to examine the factors associated with this mitochondrial introgression. A reduced representation library of over 6220 single nucleotide polymorphisms (SNPs) from the nuclear genome showed that mitochondrial introgression into H. minckleyi is biased relative to the amount of nuclear introgression. SNP assignment probabilities also indicated that cichlids with more hybrid ancestry are not more commonly female providing no support for asymmetric backcrossing or hybrid‐induced sex‐ratio distortion in generating the bias in mitochondrial introgression. Smaller effective population size in H. minckleyi inferred from the SNPs coupled with sequences of all 13 mitochondrial proteins suggests that relaxed selection on the mitogenome could be facilitating the introgression of “H. cyanoguttatus” haplotypes. Additionally, we showed that springs with colder temperatures had greater amounts of mitochondrial introgression from H. cyanoguttatus. Relaxed selection in H. minckleyi coupled with temperature‐related molecular adaptation could be facilitating mitogenomic introgression into H. minckleyi.