Cyprinodon Tularosa Research Articles

Rapid vertebrate speciation via isolation, bottlenecks, and drift

Speciation is often driven by selective processes like those associated with viability, mate choice, or local adaptation, and "speciation genes" have been identified in many eukaryotic lineages. In contrast, neutral processes are rarely considered as the primary drivers of speciation, especially over short evolutionary timeframes. Here, we describe a rapid vertebrate speciation event driven primarily by genetic drift. The White Sands pupfish (Cyprinodon tularosa) is endemic to New Mexico's Tularosa Basin where the species is currently managed as two Evolutionarily significant units (ESUs) and is of international conservation concern (Endangered). Whole-genome resequencing data from each ESU showed remarkably high and uniform levels of differentiation across the entire genome (global FST ≈ 0.40). Despite inhabiting ecologically dissimilar springs and streams, our whole-genome analysis revealed no discrete islands of divergence indicative of strong selection, even when we focused on an array of candidate genes. Demographic modeling of the joint allele frequency spectrum indicates the two ESUs split only ~4 to 5 kya and that both ESUs have undergone major bottlenecks within the last 2.5 millennia. Our results indicate the genome-wide disparities between the two ESUs are not driven by divergent selection but by neutral drift due to small population sizes, geographic isolation, and repeated bottlenecks. While rapid speciation is often driven by natural or sexual selection, here we show that isolation and drift have led to speciation within a few thousand generations. We discuss these evolutionary insights in light of the conservation management challenges they pose.

The endangered White Sands pupfish (Cyprinodon tularosa) genome reveals low diversity and heterogenous patterns of differentiation.

The White Sands pupfish (Cyprinodon tularosa), endemic to New Mexico in Southwestern North America, is of conservation concern due in part to invasive species, chemical pollution, and groundwater withdrawal. Herein, we developed a draft reference genome and use it to provide biological insights into the evolution and conservation of C. tularosa. We used our assembly to localize microsatellite markers previously used to demarcate evolutionary significant units (ESU), quantified genomic divergence and transposable element profiles between species, and compared C. tularosa genomic diversity related species. Our de novo assembly of PacBio Sequel II error-corrected reads resulted in a 1.08Gb draft genome with a contig N50 of 1.4Mb and 25,260 annotated protein coding genes, including 95% of the expected Actinopterygii conserved complete single-copy orthologues. Many of the C. tularosa microsatellite markers used for conservation assessments fell within, or near, genes and exhibited a pattern of increased heterozygosity near genic areas compared to those in intergenic regions. Nuclear alignments between these two species revealed 193genes contained in rapidly diverging tracts; transposable element profiles were largely concordant and suggest a shared, rapid expansion of LINE and Gypsy elements. Genome-wide heterozygosity was markedly lower in C. tularosa compared to estimates from other related species, probably because of smaller long-term effective population sizes constrained by their isolated and limited habitat. Overall, these inferences provide new insights into C. tularosa that should help inform future management efforts.

OCCUPANCY MODELING OF HABITAT USE BY WHITE SANDS PUPFISH AT THE MALPAIS SPRING CIÉNEGA, NEW MEXICO

We used occupancy modeling to investigate habitat use by White Sands pupfish (Cyprinodon tularosa) in a 53.4-ha cienega supported by discharge from Malpais Spring. The cienega has been subject to considerable alteration by humans over the last ca. 200 years, resulting in dynamic conditions of emergent wetland vegetation structure and composition and spatial variation in surface water characteristics. Site occupancy models were developed to describe variation in probabilities of detection and habitat use. Detection of White Sands pupfish was negatively influenced by total emergent wetland plant cover, and less so by survey-specific measurements of water temperature and cloud cover. Site occupancy, which we interpreted as habitat use because we did not assume site closure, was consistently influenced by additive effects of water depth and cover by beaked spike-rush (Eleocharis rostellata) in top-ranked models. In the top-ranked model, with other covariates set at their mean value, habitat use probability reached a plateau at 1 at a water depth of ≥30 cm, and habitat use probability fell below about 0.6 when beaked spike-rush cover was ≥0.7. The top-ranked models indicated that habitat use was also influenced to a lesser extent by chairmaker's bulrush (Schoenoplectus americanus) cover and floating algal mats. The negative effect of chairmaker's bulrush cover on habitat use probability was moderated by water depth. Application of depth and spike-rush cover criteria taken from the top-ranked model produced an estimate of 1.58 ha of high-use probability habitat in the cienega. The results have implications for monitoring the pupfish population and its habitat, and for development of reference conditions for management of the Malpais Spring cienega.

Tagging effects of passive integrated transponder and visual implant elastomer on the small-bodied white sands pupfish (Cyprinodon tularosa)

Abstract One of the greatest limiting factors of studies designed to obtain growth, movement, and survival in small-bodied fishes is the selection of a viable tag. The tag must be relatively small with respect to body size as to impart minimal sub-lethal effects on growth and mobility, as well as be retained throughout the life of the fish or duration of the study. Thus, body size of the model species becomes a major limiting factor; yet few studies have obtained empirical evidence of the minimum fish size and related tagging effects. The probability of surviving a tagging event was quantified in White Sands pupfish ( Cyprinodon tularosa ) across a range of sizes (19–60 mm) to address the hypothesis that body size predicts tagging survival. We compared tagging related mortality, individual taggers, growth, and tag retention in White Sands pupfish implanted with 8-mm passive integrated transponder (PIT), visual implant elastomer (VIE), and control (handled similarly, but no tag implantation) over a 75 d period. Initial body weight was a good predictor of the probability of survival in PIT- and VIE-tagged fish. As weight increased by 1 g, the fish were 4.73 times more likely to survive PIT-tag implantation compared to the control fish with an estimated suitable tagging size at 1.1 g (TL: 39.29 ± 0.41 mm). Likewise, VIE-tagged animals were 2.27 times more likely to survive a tagging event compared to the control group for every additional 1 g with an estimated size suitable for tagging of 0.9 g (TL: 36.9 ± 0.36 mm) fish. Growth rates of PIT- and VIE-tagged White Sands pupfish were similar to the control groups. This research validated two popular tagging methodologies in the White Sands pupfish, thus providing a valuable tool for characterizing vital rates in other small-bodied fishes.

Genetic signatures of translocations and habitat fragmentation for two evolutionarily significant units of a protected fish species

Genetic population structure was evaluated for the White Sands pupfish (Cyprinodon tularosa), a protected fish species comprised of two Evolutionarily Significant Units (ESUs); the Malpais Spring ESU and the Salt Creek ESU. The Malpais Spring ESU is restricted to Malpais Spring, whereas the Salt Creek ESU includes the native Salt Creek population and two Salt Creek-derived populations at Mound Spring and Lost River; all three of these habitats are physically fragmented. We sampled the upper and lower reaches of the four populations, examining 13 DNA microsatellite loci from 40 individuals per population. As expected, significant genetic structure was observed between the two ESUs; Malpais Spring and Salt Creek. Substantial genetic drift was observed for the introduced Lost River population, with modest genetic drift for the introduced Mound Spring population. Taken together with ecological data, neither of the introduced populations successfully replicates the Salt Creek population. We also report significant reductions in genetic diversity for the upper reaches of both Salt Creek and Lost River, indicating that recent habitat changes have altered the genetic structure of these two populations. We consider these findings along with previously reported ecological data to develop guidelines for managing C. tularosa.

Predation of a pupfish by a fishing spider subsequently stolen by a diving beetle

Abstract A State-threatened White Sands pupfish (Cyprinodon tularosa) was captured by a fishing spider (genus Dolomedes) in a spring on White Sands Missile Range, New Mexico. Before it was able to consume its prey, a predaceous diving beetle (Cybister fimbriolatus) stole the pupfish from the spider's grasp. Depredation of pupfish by these two invertebrates has not previously been documented to our knowledge. Although it is likely not a significant mortality source for pupfish populations, the pupfish is nonetheless a potential food source for Dolomedes and C. fimbriolatus.

Estimating divergence time for two evolutionarily significant units of a protected fish species

The evolutionarily significant unit concept provides a powerful tool for conserving biodiversity below the species level, but temporal criteria are often used explicitly or implicitly in the operational definitions of evolutionarily significant units (ESUs). Such temporal considerations have important implications for recently diverged taxa, as is the case with the White sands pupfish (Cyprinodon tularosa). This species consists of two native populations previously designated as the Malpais Spring and Salt Creek ESUs based on allele frequency differences at nuclear markers and their ecologically divergent habitats; despite a lack of reciprocal monophyly. Isolation of these two ESUs presumably occurred during the mid-Holocene, but an alternative hypothesis is that the populations were isolated due to changes in surface hydrology associated with overgrazing in the late 19th and early 20th centuries. We assayed 13 microsatellite loci and applied an Approximate Bayesian Computation analysis to estimate time of divergence between the two populations. Our reference table consisted of 1,000,000 simulated data sets, and we used three different models, each having different combinations of summary statistics. Estimates of median divergence time varied from approximately 6,500–11,000 generations (3,250–11,000 years). These findings support the hypothesis that Malpais Spring and Salt Creek having been isolated for a least a few millennia, and together with previously documented adaptive divergence, argues for continued management as separate conservation units. We consider the temporal constraints for defining evolutionary significance as it relates to recently diverged populations occupying ecologically divergent habitats.

Effects of Salinity on Physa acuta, the Intermediate Host for the Parasite Posthodiplostomum minimum: Implications for the Translocation of the Protected White Sands Pupfish

AbstractWe report the salinity tolerance of snails to evaluate how parasite communities with complex life cycles have been altered by translocations of the White Sands pupfish Cyprinodon tularosa to habitats with altered salinity levels. Native and introduced pupfish populations co‐occur with the gastropods Physa acuta and associated white grub parasite, Posthodiplostomum minimum, at two brackish springs (Malpais and Mound), but physids are absent from the two saline habitats occupied by White Sands pupfish. We conducted a salinity challenge experiment to test the hypothesis that environmental salinity limits the distribution of physid snails. A 22‐d survival experiment with the Malpais Spring physid population indicated that exposure to elevated salinities significantly reduced survival. We also saw sequential declines in survival and reproduction that were proportional to salinity exposure. Salinity of 7‰ was the apparent threshold for these effects. These results have implications for the use of translocation as a conservation tool in the management of fish populations.

Contemporary Evolutionary Divergence for a Protected Species following Assisted Colonization

BackgroundContemporary evolution following assisted colonization may increase the probability of persistence for refuge populations established as a bet-hedge for protected species. Such refuge populations are considered “genetic replicates” that might be used for future re-colonization in the event of a catastrophe in the native site. Although maladaptive evolutionary divergence of captive populations is well recognized, evolutionary divergence of wild refuge populations may also occur on contemporary time scales. Thus, refuge populations may lose their “value” as true genetic replicates of the native population. Here, we show contemporary evolutionary divergence in body shape in an approximately 30-year old refuge population of the protected White Sands pupfish (Cyprinodon tularosa) resulting in a body-shape mismatch with its native environment.Methodology/Principal FindingsGeometric morphometic data were collected from C. tularosa cultures raised in experimental mesocosms. Cultures were initiated with fish from the two native populations, plus hybrids, in high or low salinity treatments representing the salinities of the two native habitats. We found that body shape was heritable and that shape variation due to phenotypic plasticity was small compared to shape variation due to population source. C. tularosa from the high salinity population retained slender body shapes and fish from the low salinity population retained deep body shapes, irrespective of mesocosm salinity. These data suggest that the observed divergence of a recently established pupfish population was not explained by plasticity. An analysis of microsatellite variation indicated that no significant genetic drift occurred in the refuge population, further supporting the adaptive nature of changes in body shape. These lines of evidence suggest that body shape divergence of the refuge population reflects a case of contemporary evolution (over a 30-year period).Conclusions/SignificanceThese results suggest assisted colonization can introduce novel, and/or relaxed selection, and lead to unintended evolutionary divergence.

Phenotypic plasticity and contemporary evolution in introduced populations: evidence from translocated populations of white sands pupfish (Cyrpinodon tularosa)

AbstractContemporary evolution has been shown in a few studies to be an important component of colonization ability, but seldom have researchers considered whether phenotypic plasticity facilitates directional evolution from the invasion event. In the current study, we evaluated body shape divergence of the New Mexico State‐threatened White Sands pupfish (Cyprinodon tularosa) that were introduced to brackish, lacustrine habitats at two different time in the recent past (approximately 30 years and 1 year previously) from the same source population (saline river environment). Pupfish body shape is correlated with environmental salinity: fish from saline habitats are characterized by slender body shapes, whereas fish from fresher, yet brackish springs are deep‐bodied. In this study, lacustrine populations consisted of an approximately 30‐year old population and several 1‐year old populations, all introduced from the same source. The body shape divergence of the 30‐year old population was significant and greater than any of the divergences of the 1‐year old populations (which were for the most part not significant). Nonetheless, all body shape changes exhibited body deepening in less saline environments. We conclude that phenotypic plasticity potentially facilitates directional evolution of body deepening for introduced pupfish populations.

Specificity of the Monogenean Gyrodactylus tularosae Kritsky and Stockwell, 2005, to Its Natural Host, the White Sands Pupfish (Cyprinodon tularosa Miller and Echelle 1975)

We examined host specificity of a recently described parasite (Gyrodactylus tularosae Kritsky and Stockwell, 2005) to its natural host, the White Sands pupfish (Cyprinodon tularosa Miller and Echelle, 1975), compared with a closely related congener, the sheepshead minnow (Cyprinodon variegatus). In each of 8 replicates, 1 uninfected C. tularosa and 1 uninfected C. variegatus were exposed to 3 C. tularosa infected with G. tularosae over a 4-d exposure trial. Focal fish were subsequently isolated for 5 d to evaluate infection persistence. Experiment-wide fluke infection prevalence was 100% for C. tularosa throughout the experiment. Prevalence on C. variegatus increased to 100% by d 3 of exposure but declined in isolation to 50% on the last day of the experiment. Fluke intensity was significantly higher for C. tularosa than C. variegatus throughout the experiment. Following isolation, parasite intensity declined for both species. These data suggest that G. tularosae prefers its native host, C. tularosa, but it may be able to use C. variegatus as a transient host.

Fish habitat associations in a spatially variable desert stream

White sands pupfish Cyprinodon tularosa were sampled with minnow traps along the length of Lost River, a highly variable desert stream in New Mexico, to evaluate if their abundance, median standard length (LS) and sex ratio values differed by microhabitat variables. Habitat measurements were made in a 4 m2 area around the minnow trap. White Sands pupfish populations were primarily structured by LS. As specific conductance and surface area increased, median size of fish decreased. Shallow areas with higher specific conductance were correlated with an increased number of fish.

Assessment of Potential Impacts of Exotic Species on Populations of a Threatened Species, White Sands Pupfish, Cyprinodon tularosa

The potential impact of introduced species on rare taxa is of particular concern to conservation biologists. We evaluate the impacts of western mosquitofish (Gambusia affinis) and virile crayfish (Orconectes virilis) on experimental populations of a threatened species, the White Sands pupfish (Cyprinodon tularosa). Forty experimental pupfish populations were exposed to one of four treatments; (a) 1 crayfish, (b) 4 crayfish, (c) 5 adult mosquitofish and (d) control. Pupfish population size and biomass was monitored over the duration of one breeding season. A repeated measure multiple analysis of covariance revealed a significant effect of treatments on response variables (population size and biomass) (P<0.0001). Mosquitofish had a significant effect on population size and biomass (P=0.0330). The effect of one crayfish was not significant (P=0. 0683). However, 4 crayfish had a significant effect (P<0.0001) on population size. We use these data, along with information on environmental tolerances of crayfish and mosquitofish, to evaluate risks for specific pupfish populations. Abbreviations: CF1 – treatment with one crayfish; CF4 – treatment with 4 crayfish; ESU – ecological significant unit; MANCOVA – multiple analysis of covariance; MANOVA – multiple analysis of variance; m – meter; MF – treatment with mosquitofish; PF – control treatment – just pupfish; R – finite growth rate; SD – standard deviation; SE – standard error

NEW SPECIES OF GYRODACTYLUS (MONOGENOIDEA, GYRODACTYLIDAE) FROM THE WHITE SANDS PUPFISH, CYPRINODON TULAROSA, IN NEW MEXICO

Abstract A new species of Gyrodactylus (Monogenoidea, Gyrodactylidae) is described from the skin of the White Sands pupfish, Cyprinodon tularosa Miller and Echelle, 1975 (Cyprinodontiformes, Cyprinodontidae) from Salt Creek, White Sands Missile Range, Tularosa Basin, New Mexico. The new species is compared with the 6 species of Gyrodactylidae known to parasitize pupfish in the southern United States.

Parasites and salinity: costly tradeoffs in a threatened species

Parasites and environmental conditions can have direct and indirect effects on individuals. We explore the relationship between salinity and parasites in an endemic New Mexico State threatened fish, the White Sands pupfish (Cyprinodon tularosa). Spatial variation in salinity limits the distribution of the endemic springsnail (Juturnia tularosae) within Salt Creek, a small desert stream. The springsnail is the presumed intermediate host for trematodes that infect the White Sands pupfish, and trematode prevalence and intensity in pupfish are positively associated with the springsnail. Salinity and parasites both have negative impacts on pupfish, but in areas of high salinity, pupfish can effectively escape parasites. Pupfish trematodes were absent from sites lacking snails. At the upstream site, the absence of parasites and lower variance in salinity were correlated with larger pupfish that were in better condition than pupfish at either the middle or lower sites. Springsnails were present in the middle section, an area with moderate salinity, and all pupfish had trematodes (median abundance 847 trematodes/fish). Lipid levels and condition were lowest in fish from the middle site. Additionally, fewer older fish indicated an increased mortality rate. At the lower site, springsnails were absent due to high salinity; pupfish trematode abundance was much lower (six trematodes/fish), and fish condition was intermediate. An additional experiment revealed that snail activity and survival were significantly reduced at high salinities commonly present at the lower site. Although both high salinity and parasites significantly affect pupfish, parasites might be more detrimental.

Morphological Divergence of Native and Recently Established Populations of White Sands Pupfish (Cyprinodon tularosa)

<i>Ichthyology & Herpetology</i> (formerly <i>Copeia</i>) publishes work on the biology of fishes, amphibians, and reptiles, or work using those organisms as models for testing hypotheses of broad significance.

Experimental evidence for costs of parasitism for a threatened species, White Sands pupfish (Cyprinodon tularosa)

Summary We used field and experimental data to test if white grub parasites (Diplostomatidae) are costly to White Sands pupfish (Cyprinodon tularosa), a threatened species restricted to four sites in the Chihuahuan desert, New Mexico. Of the four populations of C. tularosa, two are native and two are introduced. The two native populations (Malpais Spring and Salt Creek) are genetically distinct and have been isolated historically in dissimilar aquatic habitats (brackish spring and saline river, respectively). Two populations were established c. 1970 from translocation of Salt Creek fish to another saline river (Lost River) and another brackish spring (Mound Spring). Physid snails (Physidae) occur in the two brackish spring habitats but not the saline river habitats. These snails are first intermediate hosts for white grubs (Diplostomatidae). Therefore, the two freshwater populations are infected by diplostomatids. For the Mound Spring population, the ecological relationship of C. tularosa and diplostomatids has only recently occurred. In 1995, a population crash occurred for C. tularosa at Mound Spring, associated with a parasite outbreak. Diplostomatids were the presumptive cause of this crash, but this was inferred from observation of infection in collected fish. Two years of seasonal sampling of the two populations revealed that all collected fish were infected. Parasite intensities were significantly lower in winter compared to summer, suggesting that heavily infected fish were lost from the population on a seasonal basis. We conducted an artificial infection experiment to assess the costs of parasitism for previously uninfected C. tularosa females for various life‐history traits. Under experimental conditions, diplostomatid infection caused increases in C. tularosa mortality and decreases in growth and fat storage. Individual‐level costs of parasitism may translate to population‐level patterns of parasitism for C. tularosa populations. Results from this study suggest that parasites may impact host overwinter survival, which is consistent with lower parasite intensities found during winters in wild populations.

Characterization of microsatellite markers in a threatened species, the White Sands pupfish (Cyprinodon tularosa)

AbstractWe report the characterization of nine new microsatellite markers for a threatened species, the White Sands pupfish (Cyprinodon tularosa), using an enriched library method. These markers show moderate levels of variation (two to five alleles per locus) in the two native populations of this species and reveal substantial divergence between these two populations as indicated by a high percentage of private alleles. These markers will prove very useful in the conservation management of this rare species.

PHOSPHOGLUCONATE DEHYDROGENASE POLYMORPHISM AND SALINITY IN THE WHITE SANDS PUPFISH.

The phosphogluconate dehydrogenase (Pgdh) locus is the only polymorphic allozyme locus observed among 37 loci examined in all four populations of a New Mexico state Endangered species, the White Sands pupfish (Cyprinodon tularosa). We report evidence suggesting that this polymorphism may be associated with salinity. Salinity levels vary widely within and between habitats occupied by White Sands pupfish. The frequency of the Pgdh100 allozyme was correlated with salinity but not with temperature. Frequency of Pgdh100 differed between low (3.76 parts per thousand (ppt)) and high (9.23 ppt) salinity sites at Malpais Spring despite no obvious barriers to fish movement. Frequencies of Pgdh100 in two introduced populations differed from that of the presumptive founding stock and correlated with salinity in the current habitats.

Phosphogluconate Dehydrogenase Polymorphism and Salinity in the White Sands Pupfish

Phosphogluconate Dehydrogenase Polymorphism and Salinity in the White Sands Pupfish