Gila Topminnow Research Articles

Development of twenty-one novel microsatellite loci for Gila topminnow, Poeciliopsis occidentalis occidentalis.

Gila topminnow (Poeciliopsis occidentalis occidentalis) was once highly abundant throughout the Lower Colorado River Basin of the southwestern United States. However, this Sonoran Desert endemic suffered extreme population declines over the past century because of habitat degradation and nonnative species introductions. Much of the prior conservation genetic work conducted on the species relied upon a small number of microsatellite loci; many exhibiting low variability in extant populations. Consequently, there was a need for additional microsatellite loci to provide high-resolution delimitation of populations for conservation purposes. Paired-end Illumina sequencing was utilized to screen the Gila topminnow genome for novel microsatellite loci. We identified 21 novel loci that exhibited no deviations from expectations of genetic equilibrium, and cross-amplified in Yaqui topminnow (P. o. sonoriensis). These loci were amplified from 401 samples representing eight populations of Gila topminnow and Yaqui topminnow. Although diversity was low for all populations (observed heterozygosity = 0.12 to 0.45), these novel markers provided ample power to identify population of origin for each individual in Bayesian assignment tests. This novel set of microsatellite loci provide a useful genetic tool to assess population genetic parameters of the endangered Gila topminnow and delineate populations for identifying conservation priorities. The cross-amplification of these loci in Yaqui topminnow shows promise for application to other Poeciliopsis species of Mexico and Central America.

Relative Inference for Paired Data: More than Meets the Eye

Relative Inference for Paired Data: More than Meets the Eye

Conservation and recovery of the Gila Topminnow in the United States

Conservation and recovery of the Gila Topminnow in the United States

Description of a previously unknown population of an endangered desert fish, Poeciliopsis occidentalis occidentalis

Abstract We report a previously unknown population of Poeciliopsis occidentalis occidentalis in La Barge Creek, a tributary stream to the Salt River in Arizona. The population inhabits a slick rock canyon with four permanent pools of water. Previous translocation efforts for P. o. occidentalis occurred more than 7 km upstream of the described location in Charlebois Spring; however, this species has not been observed at the translocation site recently. It is possible that the LaBarge Creek population emigrated from Charlebois Spring. Additional sampling is necessary to determine the source of this population.

Genetic Evaluation of Captive Populations of Endangered Species and Merging of Populations: Gila Topminnows as an Example

To avoid extinction, captive populations of a number of endangered species have been established. While in captivity, these populations have been managed to retain genetic variation although direct evaluation of this strategy using molecular markers is not common. In addition, when the number of founders for a captive population is small, other founders or populations may be added to increase genetic variation. Here we examined refugial populations of the endangered Gila topminnow (Poeciliopsis occidentalis) from 4 locations in the southwestern United States. We found that over 5 years (about 10 generations), genetic variation as measured by 5 microsatellite loci was not lost, presumably because the adult census population size was 500 or greater. In addition, some variation not initially observed was observed later. Some of these variants may have been missed because of sampling but it appears that some may have been contributed by new mutations. In addition, 2 populations of successfully merged ancestry from the 4 source populations were examined. Based on population-specific markers and a quantitative evaluation of ancestry using a likelihood approach, it appears that ancestry from each of the source populations was retained in both populations.

Conservation genetics and evolution in an endangered species: research in Sonoran topminnows*

Conservation genetics of endangered species has primarily focused on using neutral markers to determine units of conservation and estimating evolutionary parameters. Because the endangered Sonoran topminnow can be bred in the laboratory and has a relatively short generation length, experiments to examine both detrimental and adaptive variations are also possible. Here, we discuss over two decades of empirical and experimental observations in the Sonoran topminnow. Results from this research have been used to determine species and evolutionary significant units using neutral markers, document inbreeding and outbreeding depression and genetic load using experimental crosses, and measure adaptive differences in fitness-related traits and variation in pathogen resistance among populations and major histocompatibility complex genotypes. In addition, both premating and postmating reproductive isolation between Gila and Yaqui topminnows have been experimentally determined, and the predicted and observed ancestry of these two species in experimental crosses has been examined over time. Although some have suggested that endangered species are unsuitable for experimentation because of both practical and ethical considerations, these results demonstrate that in this case an endangered species can be employed to examine fundamental questions in conservation and evolution.

Interactions between Desert Pupfish and Gila Topminnow Can Affect Reintroduction Success

AbstractIn fisheries, recovery actions for species of concern sometimes involve reintroductions of multiple species. As an example, desert pupfish Cyprinodon macularius and Gila topminnow Poeciliopsis occidentalis historically had sympatric distributions and inhabited similar environments, and they are often reintroduced into the same waters. Success of these stockings has varied greatly, and a hypothesis developed among conservationists that desert pupfish populations were more likely to establish and persist if they were stocked first and allowed to establish before Gila topminnow were stocked. We examined historical records of desert pupfish reintroductions and conducted laboratory experiments to evaluate this hypothesis. For the reintroductions, we evaluated 29 ponds where four general stocking strategies (treatments) were implemented: (1) only desert pupfish were stocked, (2) desert pupfish were stocked first and allowed to establish and then Gila topminnow were stocked, (3) both desert pupfish and Gila topminnow were stocked simultaneously, and (4) Gila topminnow were stocked first and allowed to establish before desert pupfish were stocked. Desert pupfish established populations and persisted in 100% of desert pupfish‐only and desert pupfish‐first ponds and 57% of simultaneous‐stocking and Gila topminnow‐first ponds. In laboratory experiments utilizing 2.4‐m‐diameter tanks, the same four treatments plus one additional treatment (in which only Gila topminnow were stocked) were implemented; each treatment was replicated four times. Desert pupfish abundance increased in 75% of the desert pupfish‐only trials and 50% of the desert pupfish‐first trials but decreased in 75% of simultaneous‐stocking trials and 100% of Gila topminnow‐first trials. Gila topminnow increased in abundance in all treatments and trials but increased the least when desert pupfish were stocked first. Our results support the original hypothesis and emphasize the need to evaluate species interactions in multiple‐species reintroductions. To increase success, desert pupfish should be stocked in isolation or stocked first and allowed to establish before Gila topminnow are stocked.Received July 12, 2011; accepted August 30, 2011

Captive Breeding of Endangered Yaqui Topminnow and Yaqui Chub for Recovery Purposes

AbstractYaqui topminnow Poeciliopsis occidentalis sonoriensis and Yaqui chub Gila purpurea, two federally endangered fishes from the Rio Yaqui basin (Arizona, USA, and Sonora, Mexico), were propagated by various methods. Propagation of Yaqui topminnow was attempted in aquaria and wading pools; the greatest number of offspring was produced in 556‐L, plastic wading pools. We added substrate, artificial plants, and a vertical mesh barrier to create refuge for offspring. Fish were stocked when water was 19°C; after 1 month, when water temperatures exceeded 21°C, Yaqui topminnow started to produce young continuously. On average, 7.4 offspring/d were captured from four pools collectively. Yaqui chub were propagated in 189‐L, glass aquaria. We manipulated photoperiod, diet, and substrate to induce spawning of Yaqui chub, but success was only achieved after the water was chilled to 17°C for 30 d and then adjusted to 21°C over 14 d. After the water was maintained at 21°C for 3 d, we covered the bottom of each aquarium with glazed ceramic tiles and a raised plastic grid to protect eggs from predation. Broadcast spawning of Yaqui chub occurred at night; the next morning, we retrieved the tiles and the attached eggs and placed them in incubation tanks. Yaqui chub eggs hatched over the next 5 d, and the hatching success rate averaged 83%. After this initial spawn, manipulation of water temperature was not required to induce spawning, as Yaqui chub spawned each time tiles were placed in the tanks. These methods worked well, and we recommend them for propagation of Yaqui topminnow and Yaqui chub.

Comparison of Upper Thermal Tolerances of Native and Nonnative Fish Species in Arizona

AbstractWe used a lethal thermal method to estimate the upper thermal tolerances of 11 native and 7 nonnative fish species found throughout southern Arizona. Fish were acclimated to 25°C and 30°C. For all species tested, an increase in acclimation temperature resulted in a higher thermal tolerance value. Among the species acclimated to 25°C, desert pupfish Cyprinodon macularius, western mosquitofish Gambusia affinis, and Gila topminnow Poeciliopsis occidentalis were most tolerant to high temperature. Speckled dace Rhinichthys osculus, spikedace Meda fulgida, and loach minnow R. cobitis were least tolerant. Many native species demonstrated a limited ability to extend their upper temperature tolerances via acclimation. Our data suggest that several native species may be sensitive to increasing annual and large daily temperature fluctuations in Arizona's streams and rivers. Although southwestern native fishes were previously believed to be tolerant to high temperature due to their evolution in desert environments, this study suggests that many of these fishes are less tolerant than previously thought. In addition, many fishes introduced from the eastern United States had higher temperature tolerances than some of the native desert species tested. Increases in stream temperatures in Arizona could reduce the habitat available for native fishes and therefore may favor those nonnative species with higher thermal tolerances.

USING SURVIVAL ANALYSIS TO STUDY TRANSLOCATION SUCCESS IN THE GILA TOPMINNOW (POECILIOPSIS OCCIDENTALIS)

Translocation, the intentional release of captive-propagated and/or wild-caught animals into the wild in an attempt to establish, reestablish, or augment a population, is a commonly used approach to species conservation. Despite the frequent mention of translocation as an aid in threatened or endangered species recovery plans, translocations have resulted in the establishment of few sustainable populations. To improve the effectiveness of translocation efforts, it is essential to identify and adopt features that contribute to successful translocations. This study analyzed 148 translocations of the endangered Gila topminnow (Poeciliopsis occidentalis) to identify various factors that have significantly influenced translocation success. We quantified success as the "persistence time" of translocated populations and used survival analysis to interpret the role of several factors. The following factors affected persistence times of translocated populations: season in which the fish were translocated, habitat type of the translocation site, and genetic origin of the fish stocked. In general, factors associated with stocking, the population stocked, and the site of translocation can significantly affect the persistence of translocated populations and thus increase the probability of translocation success. For Gila topminnow, future translocations should be undertaken in late summer or fall (not early summer), should occur into ponds (not streams, wells, or tanks), and should generally utilize individuals from genetic lineages other than Monkey Spring. For other species, a key lesson emerging from this work is that life history attributes for each translocated species need to be considered carefully.

COMPARISON OF GILA TOPMINNOW AND WESTERN MOSQUITOFISH AS BIOLOGICAL CONTROL AGENTS OF MOSQUITOES

I compared acute tolerance of Gila topminnow, Poeciliopsis occidentalis, and western mosquitofish, Gambusia affinis, to ammonia and high water temperature and also compared diet, food selectivity, and impact on invertebrate populations to evaluate the potential for each species to effectively control mosquitoes (Culicidae) in wetland habitats. Critical thermal maxima differed among species, sexes, and lifestages, but these differences were likely not biologically significant due to their small magnitude and the ability of wild populations of both species to adapt to high temperatures. In 24-hour tests, G. affinis displayed about twice the ammonia tolerance as did P. occidentalis. However, long-term survival in habitats with high ammonia concentrations is questionable, thus reducing the perceived benefit of using G. affinis for mosquito abatement in these habitats. Diet overlap was significant between sexes within species but was not significant between species. However, both species exhibited significant dietary selection for mosquito larvae and pupae under experimental conditions. Shared dietary preference for mosquito larvae and pupae, in addition to similarity in temperature tolerance between species, suggests that P. occidentalis, a native and historically widespread species, can be used in place of nonnative G. affinis for mosquito control. There is no evidence to suggest that nonnative G. affinis is better suited for mosquito abatement, and since G. affinis is replacing P. occidentalis throughout the native species' former range, it should no longer be introduced into the Gila River basin for mosquito control. However, managers who would use P. occidentalis for mosquito abatement must take care not to interfere with conservation efforts by disrupting the genetic structure of natural populations of P. occidentalis.

The endangered Sonoran topminnow: Examination of species and ESUs using three mtDNA genes

There has been controversy over the species status of Sonoran topminnows and debate about the presence of ESUs in the Gila topminnow. From examination of sequence variation at 2626 base pairs over three mtDNA genes, we found a 29 (1.1%) nucleotide genetic difference between Gila and Yaqui topminnows. This provides strong support that these two taxa are separate species, Poeciliopsis occidentalis (Gila topminnow) and P. sonoriensis (Yaqui topminnow) and have been separated for approximately one million years. All the Gila topminnows within Arizona have the same sequence for the three mtDNA genes, that is, there is not reciprocal monophyly for mtDNA sequence data for the two previously designated ESUs. However, evidence of the unique habitat for Monkey Spring, its long-term isolation from other Gila topminnow habitats, and the presence of unique fish and invertebrate taxa in Monkey Spring support the designation of the Monkey Spring topminnows as an ESU. Finally, theoretical considerations using molecular data and estimates of heterozygosity and genetic distance for nuclear genes between populations of the Gila topminnow show that the lack of mtDNA variation is not inconsistent with the level and pattern of nuclear genetic variation observed.

Premating, Not Postmating, Barriers Drive Genetic Dynamics in Experimental Hybrid Populations of the Endangered Sonoran Topminnow

The timing and pattern of reproductive barrier formation in allopatric populations has received much less attention than the accumulation of reproductive barriers in sympatry. The theory of allopatric speciation suggests that reproductive barriers evolve simply as by-products of overall genetic divergence. However, observations of enhanced premating barriers in allopatric populations suggest that sexual selection driven by intraspecific competition for mates may enhance species-specific signals and accelerate the speciation process. In a previous series of laboratory trials, we examined the strength of premating and postmating barriers in an allopatric species pair of the endangered Sonoran topminnow, Poeciliopsis occidentalis and P. sonoriensis. Behavioral observations provided evidence of asymmetrical assortative mating, while reduced brood sizes and male-biased F(1) sex ratios suggest postmating incompatibilities. Here we examine the combined effects of premating and postmating barriers on the genetic makeup of mixed populations, using cytonuclear genotype frequencies of first- and second-generation offspring. Observed genotype frequencies strongly reflect the directional assortative mating observed in behavioral trials, illustrating how isolating barriers that act earlier in the reproductive cycle will have a greater effect on total reproductive isolation and may be more important to speciation than subsequent postmating reproductive barriers.

Assessing Contaminant Sensitivity of Endangered and Threatened Aquatic Species: Part III. Effluent Toxicity Tests

Toxicity tests using standard effluent test procedures described by the U.S. Environmental Protection Agency were conducted with Ceriodaphnia dubia, fathead minnows (Pimephales promelas), and seven threatened and endangered (listed) fish species from four families: (1) Acipenseridae: shortnose sturgeon (Acipenser brevirostrum); (2) Catostomidae; razorback sucker (Xyrauchen texanus); (3) Cyprinidae: bonytail chub (Gila elegans), Cape Fear shiner (Notropis mekistocholas) Colorado pikeminnow (Ptychocheilus lucius), and spotfin chub (Cyprinella monacha); and (4) Poecillidae: Gila topminnow (Poeciliopsis occidentalis). We conducted 7-day survival and growth studies with embryo-larval fathead minnows and analogous exposures using the listed species. Survival and reproduction were also determined with C. dubia. Tests were conducted with carbaryl, ammonia--or a simulated effluent complex mixture of carbaryl, copper, 4-nonylphenol, pentachlorophenol and permethrin at equitoxic proportions. In addition, Cape Fear shiners and spotfin chub were tested using diazinon, copper, and chlorine. Toxicity tests were also conducted with field-collected effluents from domestic or industrial facilities. Bonytail chub and razorback suckers were tested with effluents collected in Arizona whereas effluent samples collected from North Carolina were tested with Cape Fear shiner, spotfin chub, and shortnose sturgeon. The fathead minnow 7-day effluent test was often a reliable estimator of toxic effects to the listed fishes. However, in 21 % of the tests, a listed species was more sensitive than fathead minnows. More sensitive species results varied by test so that usually no species was always more or less sensitive than fathead minnows. Only the Gila topminnow was consistently less sensitive than the fathead minnow. Listed fish species were protected 96% of the time when results for both fathead minnows and C. dubia were considered, thus reinforcing the value of standard whole-effluent toxicity tests using those two species. If the responses of specific listed species are important for management decisions, our study supports the value in developing culture and testing procedures for those species.

Mating behaviour in the endangered Sonoran topminnow: speciation in action

Two species of the endangered Sonoran topminnow, Poeciliopsis occidentalis and P. sonoriensis, occur in two isolated drainage systems in southeast Arizona, U.S.A., and are allopatric throughout their range. Although these two taxa are morphologically very similar, and have been previously described as the same species or subspecies, several molecular studies have since indicated that they differ more than their morphology suggests. To determine whether the behaviours of the two species function as premating barriers to reproduction, we investigated their mating preferences and behavioural patterns in a laboratory setting. Results from no-choice mating observations showed that the mating behaviours of the two species differ. Observations conducted during multiple-choice mating trials provided evidence of assortative mating, suggesting an early stage of premating reproductive isolation.

Genetic variation and resistance to a bacterial infection in the endangered Gila topminnow

AbstractWe tested the association between host genetic diversity and resistance to a novel pathogen using controlled experiments to compare bacterially induced mortality among four populations of the endangered Gila topminnow (Poeciliopsis occidentalis) with different levels of genetic diversity, and between nine lines of inbred topminnows and their respective (non‐inbred) source populations. We exposed fish in treatment groups to salinity shock and high concentrations of the bacterium Listonella (Vibrio) anguillarum, a causative agent of vibriosis in fish. Mortality associated with vibriosis (mortality) 1 to 6 days post‐exposure differed among the populations, and between inbred and non‐inbred samples. However, mortality was not associated with expected heterozygosity based on microsatellite loci diversity, nor was it associated with expected or observed heterozygosity at a major histocompatibility complex (MHC) class II locus. Neither was mortality related to the presence or absence of specific MHC alleles. Additionally, the effect of severe inbreeding was to reduce mortality in the inbred fish relative to the non‐inbred controls in every population. Taken in the context of other studies, we conclude that effects of genetic diversity may be context‐ and locus‐specific, environmental stress may be an important determinant of host immunity, and genetic diversity should be used cautiously to predict the potential response of a population to a specific environmental challenge.

Differences in Swimming Ability and Behavior in Response to High Water Velocities among Native and Nonnative Fishes

We conducted swimming performance tests on native and nonnative fishes commonly found in Arizona streams to evaluate the extent of differences in swimming ability among species. Fishes with similar mean lengths were subjected to stepwise increases in water velocity in a laboratory swim tunnel until fish could no longer maintain position. Nonnative fathead minnows Pimephales promelas and red shiners Cyprinellalutrensis exhibited swimming abilities similar to native longfin dace Agosia chrysogaster, speckled dace Rhinichthys osculus and spikedace Meda fulgida. Nonnative mosquitofish Gambusia affinis exhibited swimming ability similar to native Gila topminnows Poeciliopsis occidentalis. Desert suckers Catostomus clarki, bluehead suckers Catostomus discobolus and speckled dace exhibited behavioral responses to high water velocities that may confer energetic advantages in swift water. Differences in swimming ability do not appear to adequately explain the disproportionate removal of nonnative fishes via flooding. Behavioral responses to high flows are more likely the mechanism that allows native fish to persist in streams during flood events.

MHC variation and tissue transplantation in fish.

Major histocompatibility complex (MHC) genes were originally discovered because of their role in tissue rejection in mammals and have subsequently been implicated in the incidence of autoimmune diseases and resistance to infectious diseases. Here we present the first demonstration that a gene defined by molecular sequence in the fish MHC, specifically a class II locus, plays an important role in tissue rejection. This effect in the endangered Gila topminnows appears to be additive and depends on the number of MHC alleles shared between the host and the recipient fish of the scale transplants. In addition, there was lower success of scale transplants in MHC-matched individuals in a population with high microsatellite variation than in a population with low variation. This suggests that other loci, presumably other MHC loci, play a significant role in transplantation success in fishes, as they do in mammals.

Using microsatellite and MHC variation to identify species, ESUs, and MUs in the endangered Sonoran topminnow.

Highly variable loci can provide insight into the recognition of species, evolutionarily significant units (ESUs) and management units (MUs). In general, the ESU and MU categories are thought to be reflective of adaptive differences between them. Here we examine this premise by presenting a comprehensive examination of genetic variation for both microsatellite loci and a major histocompatibility complex (MHC) locus, thought to be of adaptive significance, in the endangered Sonoran topminnow. The extent of variation for the microsatellite loci and the MHC gene within the 13 populations of the Gila topminnow is highly correlated, suggesting that nonselective factors have played an important role in influencing variation within and between populations for the MHC locus. Therefore, using all of these loci, we found that the eight natural populations of the Gila topminnow fell into two different ESUs, one of which had four different MUs. The source of the Boyce Thompson sample, a population that was used extensively for restocking, appeared to be Monkey Spring. The source of the Watson Wash population also appeared to be Monkey Spring (or Boyce Thompson). The newly colonized Santa Cruz River population, which had the most genetic variation of any Gila topminnow population, appeared to descend primarily from Sonoita Creek populations. The Yaqui topminnow, presently considered another subspecies of the Sonoran topminnow, was very distinct for both microsatellite (only two of 25 alleles found in the Yaqui were in any of the Gila topminnow samples) and MHC alleles (nonoverlapping sets of alleles for the two groups). As a result, it appeared that the taxonomic status of the two subspecies should be re-evaluated and that full species status for Gila and Yaqui topminnows was appropriate. There was evidence for the importance of long-term selection at the MHC locus in the higher rate of nonsynonymous than synonymous substitution. In addition, there appeared to have been a duplication of the MHC locus that was present in most of the fish in six of the natural populations of the Gila topminnow.

Parasite resistance and genetic variation in the endangered Gila topminnow

AbstractIn recent years, it has become apparent that introduced or novel pathogens or parasites may have a significant negative impact on endangered species. Here we examine experimentally the effect of an exotic fluke from guppies on the endangered Gila topminnow. Populations from different sources showed variable responses (although statistically non‐significant) to the fluke and, in particular, the most homozygous population had high fluke infections and high subsequent mortality. Homozygotes for a MHC (major histocompatibility complex) gene had lower (although statistically non‐significant) survival when infected with flukes than did heterozygotes. An inbred line from one of the populations had statistically significant lower survival and higher fluke infection than did a simultaneous outbred control. Overall, Gila topminnows appear quite susceptible to infection by the non‐native fluke compared to other related species. In addition, it was shown that Gila topminnows can be infected by casual contact with infected guppies. This is another example of the potential detrimental effects of a parasite on an endangered species, a threat that may constitute a particular problem for species with low genetic variation, either in general, for important MHC genes, or for populations with a past history of inbreeding.