Parsing variance by marker type: Testing biogeographic hypotheses and differential contribution of historical processes to population structure in a desert lizard.

A fundamental goal of population genetic studies is to identify historical biogeographic patterns and understand the processes that generate them. However, localized demographic events can skew population genetic inference. Assessing populations with multiple types of genetic markers, each with unique mutation rates and responses to changes in population size, can help to identify potentially confounding population-specific demographic processes. Here, we compared population structure and connectivity inferred from microsatellites and restriction site-associated DNA loci among 17 populations of an arid-specialist lizard, the desert night lizard, Xantusia vigilis, in central California to test among historical processes structuring population genetic diversity. We found that both marker types yielded generally concordant insights into population genetic structure including a major phylogenetic break maintained between two populations separated by less than 10 km, suggesting that either marker type could be used to understand generalized demographic patterns across the region for management purposes. However, we also found that the effects of demography on marker discordance could be used to elucidate population histories and distinguish among competing biogeographic hypotheses. Our results suggest that comparisons of within-population diversity across marker types provide powerful opportunities for leveraging marker discordance, particularly for understanding the creation and maintenance of contact zones among clades.

In the surf zone: Reproductive strategy of the calico surfperch (Amphistichus koelzi) in a comparative context.

We examined the reproductive life history of calico surfperch (Amphistichus koelzi), including mating season, pregnancy, gestation and multiple paternity utilizing restriction site-associated DNA sequencing. Furthermore, we compared the mating season of calico with barred (Amphistichus argenteus), walleye (Hyperprosopon argenteum) and silver (Hyperprosopon ellipticum) surfperches to determine if the timing of reproduction is divergent within and between the genera. In calico surfperch, the mating season occurs from October to November, and females gestate from December to May. All broods exhibit multiple paternity with a range of four to seven sires per brood. The mating season of calico overlaps completely with barred surfperch; however, barred surfperches have a protracted mating season which extends until the beginning of December, which may be due to differences in reproductive strategy such as size at first reproduction. In the genus, the Hyperprosopon mating season begins earlier than Amphistichus, with divergence in the onset of mating between Hyperprosopon congeners of approximately 1 month.

Use of stochastic patch occupancy models in the California red-legged frog for Bayesian inference regarding past events and future persistence.

Assessing causes of population decline is critically important to management of threatened species. Stochastic patch occupancy models (SPOMs) are popular tools for examining spatial and temporal dynamics of populations when presence-absence data in multiple habitat patches are available. We developed a Bayesian Markov chain method that extends existing SPOMs by focusing on past environmental changes that may have altered occupancy patterns prior to the beginning of data collection. Using occupancy data from 3 creeks, we applied the method to assess 2 hypothesized causes of population decline-in situ die-off and residual impact of past source population loss-in the California red-legged frog. Despite having no data for the 20-30 years between the hypothetical event leading to population decline and the first data collected, we were able to discriminate among hypotheses, finding evidence that in situ die-off increased in 2 of the creeks. Although the creeks had comparable numbers of occupied segments, owing to different extinction-colonization dynamics, our model predicted an 8-fold difference in persistence probabilities of their populations to 2030. Adding a source population led to a greater predicted persistence probability than did decreasing the in situ die-off, emphasizing that reversing the deleterious impacts of a disturbance may not be the most efficient management strategy. We expect our method will be useful for studying dynamics and evaluating management strategies of many species.

Uso de Modelos Estocásticos de Ocupación de Fragmentos de la Rana Californiana de Patas Rojas para la Inferencia Bayesiana con Respecto a Eventos Pasados y su Persistencia en el Futuro Resumen La evaluación de las causas de la declinación poblacional es de importancia crítica para el manejo de especies amenazadas. Los modelos estocásticos de ocupación de parches (SPOMs, en inglés) son herramientas populares para examinar las dinámicas espaciales y temporales de las poblaciones cuando están disponibles los datos de presencia-ausencia para múltiples parches de hábitat. Desarrollamos un método bayesiano de cadena de Markov que extiende a los SPOMs existentes al enfocarse en los cambios ambientales pasados que podrían haber alterado los patrones de ocupación previos al inicio de la recolección de datos. Con los datos de ocupación de tres arroyos, aplicamos este método para evaluar dos causas hipotéticas de la declinación poblacional - muerte in situ e impacto residual de causas anteriores de pérdida de una poblacion fuente - de la rana californiana de patas rojas. A pesar de no tener datos para 20 - 30 años entre el evento hipotético que derivó en la declinación poblacional y los primeros datos recolectados, pudimos discriminar entre las hipótesis, encontrando evidencia de que la muerte in situ incrementó en dos de los arroyos. Aunque los arroyos tuvieron un número comparable de segmentos ocupados, debido a diferentes dinámicas de colonización - extinción, nuestro modelo predijo una diferencia ocho veces mayor en las probabilidades de persistencia de las poblaciones hasta el 2030. La suma de una población fuente resultó en una mayor probabilidad de persistencia pronosticada que con la reducción de la muerte in situ, enfatizando que la reversión de los impactos dañinos de una perturbación puede no ser la mejor estrategia de manejo. Esperamos que nuestro método sea útil para el estudio de las dinámicas y para la evaluación de las estrategias de manejo de muchas especies.

Historical Population Size Change and Differentiation of Relict Populations of the Endangered Giant Kangaroo Rat.

From a conservation management perspective it is important to understand how genetic diversity is partitioned across a species' range, including 1) identification of evolutionarily distinct units versus those recently isolated through anthropogenic activities and 2) the relative genetic contributions among components of fragmented (meta)populations. To address these questions, we investigated the phylogeography and metapopulation structure among relict populations of the endangered giant kangaroo rat (Dipodomys ingens) in the highly altered San Joaquin Desert Ecosystem. This keystone species underwent a ~97% range reduction over the past century, resulting in a current range that is highly fragmented, with 2 dominant northern and southern populations occurring 150 km apart. We sequenced >800 bp of mitochondrial DNA and genotyped 17 nuclear microsatellites in >275 D. ingens to assess the evolutionary relationship of these populations as well as the genetic structure within the northern metapopulation. A Bayesian Skyline Plot indicated that the species experienced a demographic expansion toward the end of the Pleistocene, with a recent population decline. Northern and southern D. ingens split 1857-13 443 years ago, prior to the massive conversion of the San Joaquin Valley to irrigated agriculture. We recommend that the northern and southern populations of D. ingens be re-classified as distinct population segments under the United States Endangered Species Act. We also observed population structure and asymmetrical migration within northern D. ingens where the Tumey Hills acted as a source contributing gene flow to all peripheral populations. This emphasized the importance of this location in the conservation of the metapopulation as a whole.

Persistence of historical population structure in an endangered species despite near-complete biome conversion in California's San Joaquin Desert.

Genomic responses to habitat conversion can be rapid, providing wildlife managers with time-limited opportunities to enact recovery efforts that use population connectivity information that reflects predisturbance landscapes. Despite near-complete biome conversion, such opportunities may still exist for the endemic fauna and flora of California's San Joaquin Desert, but comprehensive genetic data sets are lacking for nearly all species in the region. To fill this knowledge gap, we studied the rangewide population structure of the endangered blunt-nosed leopard lizard Gambelia sila, a San Joaquin Desert endemic, using restriction site-associated DNA (RAD), microsatellite and mtDNA data to test whether admixture patterns and estimates of effective migration surfaces (EEMS) can identify land areas with high population connectivity prior to the conversion of native xeric habitats. Clustering and phylogenetic analyses indicate a recent shared history between numerous isolated populations and EEMS reveals latent signals of corridors and barriers to gene flow over areas now replaced by agriculture and urbanization. Conflicting histories between the mtDNA and nuclear genomes are consistent with hybridization with the sister species G. wislizenii, raising important questions about where legal protection should end at the southern range limit of G. sila. Comparative analysis of different data sets also adds to a growing list of advantages in using RAD loci for genetic studies of rare species. We demonstrate how the results of this work can serve as an evolutionary guidance tool for managing endemic, arid-adapted taxa in one of the world's most compromised landscapes.

Multilocus sequence data reveal dozens of putative cryptic species in a radiation of endemic Californian mygalomorph spiders (Araneae, Mygalomorphae, Nemesiidae).

We use mitochondrial and multi-locus nuclear DNA sequence data to infer both species boundaries and species relationships within California nemesiid spiders. Higher-level phylogenetic data show that the California radiation is monophyletic and distantly related to European members of the genus Brachythele. As such, we consider all California nemesiid taxa to belong to the genus Calisoga Chamberlin, 1937. Rather than find support for one or two taxa as previously hypothesized, genetic data reveal Calisoga to be a species-rich radiation of spiders, including perhaps dozens of species. This conclusion is supported by multiple mitochondrial barcoding analyses, and also independent analyses of nuclear data that reveal general genealogical congruence. We discovered three instances of sympatry, and genetic data indicate reproductive isolation when in sympatry. An examination of female reproductive morphology does not reveal species-specific characters, and observed male morphological differences for a subset of putative species are subtle. Our coalescent species tree analysis of putative species lays the groundwork for future research on the taxonomy and biogeographic history of this remarkable endemic radiation.

Hydric physiology and ecology of a federally endangered desert lizard.

Animals can respond to extreme climates by behaviourally avoiding it or by physiologically coping with it. We understand behavioural and physiological thermoregulation, but water balance has largely been neglected. Climate change includes both global warming and changes in precipitation regimes, so improving our understanding of organismal water balance is increasingly urgent. We assessed the hydric physiology of US federally endangered blunt-nosed leopard lizards (Gambelia sila) by measuring cutaneous evaporative water loss (CEWL), plasma osmolality and body condition. Measurements were taken throughout their active season, the short period of year when these lizards can be found aboveground. Compared to a more mesic species, G. sila had low CEWL which is potentially desert-adaptive, and high plasma osmolality that could be indicative of dehydration. We hypothesized that throughout the G. sila active season, as their habitat got hotter and drier, G. sila would become more dehydrated and watertight. Instead, CEWL and plasma osmolality showed minimal change for females and non-linear change for males, which we hypothesize is connected to sex-specific reproductive behaviours and changes in food availability. We also measured thermoregulation and microhabitat use, expecting that more dehydrated lizards would have lower body temperature, poorer thermoregulatory accuracy and spend less time aboveground. However, we found no effect of CEWL, plasma osmolality or body condition on these thermal and behavioural metrics. Finally, G. sila spends considerable time belowground in burrows, and burrows may serve not only as essential thermal refugia but also hydric refugia.

Shrub density effects on the presence of an endangered lizard of the Carrizo Plain National Monument, California.

Positive associations between animals and foundational shrub species are frequent in desert ecosystems for shelter, resources, refuge, and other key ecological processes. Herein, we tested the impact of the density of the shrub species Ephedra californica on the presence and habitat use of the federally endangered lizard species, Gambelia sila. To do this, we used a 3-year radio telemetry dataset and satellite-based counts of shrub density across sites at the Carrizo Plain National Monument in San Luis Obispo County, CA. The effect of shrub density on lizard presence was contrasted with previous shrub cover analyses to determine whether measures of shrub density were superior to shrub cover in predicting lizard presence. Increasing shrub density increased lizard presence. As shrub density increased, lizards were located more frequently "above ground" versus "below ground" in burrows. Male lizards had significantly larger home ranges than females, but both sexes were similarly associated with increasing shrub densities. Shrub density and shrub cover models did not significantly differ in their prediction of lizard presence. These findings suggest that both habitat measures are effective analogs and that ecologically, both cover and the density of foundation shrub species are key factors for some desert lizards.

Habitat heterogeneity affects the thermal ecology of an endangered lizard.

Global climate change is already contributing to the extirpation of numerous species worldwide, and sensitive species will continue to face challenges associated with rising temperatures throughout this century and beyond. It is especially important to evaluate the thermal ecology of endangered ectotherm species now so that mitigation measures can be taken as early as possible. A recent study of the thermal ecology of the federally endangered Blunt-nosed Leopard Lizard (Gambelia sila) suggested that they face major activity restrictions due to thermal constraints in their desert habitat, but that large shade-providing shrubs act as thermal buffers to allow them to maintain surface activity without overheating. We replicated this study and also included a population of G. sila with no access to large shrubs to facilitate comparison of the thermal ecology of G. sila populations in shrubless and shrubbed sites. We found that G. sila without access to shrubs spent more time sheltering inside rodent burrows than lizards with access to shrubs, especially during the hot summer months. Lizards from a shrubbed site had higher midday body temperatures and therefore poorer thermoregulatory accuracy than G. sila from a shrubless site, suggesting that greater surface activity may represent a thermoregulatory trade-off for G. sila. Lizards at both sites are currently constrained from using open, sunny microhabitats for much of the day during their short active seasons, and our projections suggest that climate change will exacerbate these restrictions and force G. sila to use rodent burrows for shelter even more than they do now, especially at sites without access to shrubs. The continued management of shrubs and of burrowing rodents at G. sila sites is therefore essential to the survival of this endangered species.

Quantitative genetics of pigmentation development in 2 populations of the common garter snake, Thamnophis sirtalis.

The evolutionary importance of ontogenetic change has been noted since Darwin. However, most analyses of phenotypic evolution focus on single landmark ages. Here, we present an inheritance study that quantifies genetic variation in pigmentation across early-age (i.e., birth to 180 days) development in 2 populations of the common garter snake, Thamnophis sirtalis. The populations are phenotypically distinct and geographically isolated (Manitoba, CA and Northern California, USA). There were highly significant differences between populations for the developmental trajectory of mean pigmentation, with the Manitoba population exhibiting a mean pigmentation level that increased across ontogeny, whereas the California population exhibited mean pigmentation that was invariant across ontogeny. Subsequent quantitative genetic analyses revealed heritable variation at all ages in Manitoba but low levels of phenotypic and genetic variation in California at all ages. A quantitative genetic decomposition of the longitudinal genetic variance-covariance matrix for the age-specific pigmentation phenotypes in the Manitoba population revealed 2 primary orthogonal axes that explained most ( approximately 100%) of the pigmentation variation across ontogeny. The primary axis, explaining 93% of the genetic variation, is an axis of genetic variation whose principal value loadings change from positive to negative across development, suggesting that the most rapid evolutionary response to selection on pigmentation variation will occur in the direction characterized by a tradeoff in early-age versus late-age pigmentation phenotypes. Pigmentation is known to be ecologically important and subject to rapid evolution under selection. Our study shows that significant differences exist between these 2 populations for their capacity to respond to selection on pigmentation which is not only influenced by the population of origin but also by the developmental process. We suggest that developmental timing may be a potential explanatory mechanism for the difference between the populations.

Habitat restoration opportunities, climatic niche contraction, and conservation biogeography in California's San Joaquin Desert.

A recent global trend toward retirement of farmland presents opportunities to reclaim habitat for threatened and endangered species. We examine habitat restoration opportunities in one of the world's most converted landscapes, California's San Joaquin Desert (SJD). Despite the presence of 35 threatened and endangered species, agricultural expansion continues to drive habitat loss in the SJD, even as marginal farmland is retired. Over the next decades a combination of factors, including salinization, climate change, and historical groundwater overdraft, are projected to lead to the retirement of more than 2,000 km2 of farmland in the SJD. To promote strategic habitat protection and restoration, we conducted a quantitative assessment of habitat loss and fragmentation, habitat suitability, climatic niche stability, climate change impacts, habitat protection, and reintroduction opportunities for an umbrella species of the SJD, the endangered blunt-nosed leopard lizard (Gambelia sila). We use our suitability models, in conjunction with modern and historical land use maps, to estimate the historical and modern rate of habitat loss to development. The estimated amount of habitat lost since the species became protected under endangered species law in 1967 is greater than the total amount of habitat currently protected through public ownership and conservation easement. We document climatic niche contraction and associated range contraction away from the more mesic margins of the species' historical distribution, driven by the anthropogenic introduction of exotic grasses and forbs. The impact of exotic species on G. sila range dynamics appears to be still unfolding. Finally, we use NASA fallowed area maps to identify 610 km2 of fallowed or retired agricultural land with high potential to again serve as habitat. We discuss conservation strategies in light of the potential for habitat restoration and multiple drivers of ongoing and historical habitat loss.

A test of desert shrub facilitation via radiotelemetric monitoring of a diurnal lizard.

Preservation of desert ecosystems is a worldwide conservation priority. Shrubs can play a key role in the structure of desert communities and can function as foundation species. Understanding desert shrub ecology is therefore an important task in desert conservation. A useful model for the function of shrubs in deserts is ecological facilitation, which explores benefits that shrubs confer on their community. Facilitation has been well developed in the context of shrub-plant interactions but less well studied for plant-animal interactions. We used radiotelemetry to test the hypothesis that a dominant desert shrub facilitates one species of diurnal lizard. We hypothesized that the blunt-nosed leopard lizard Gambelia sila would spend some part of its daily activity cycle associated with California jointfir Ephedra californica, and that lizard association with shrubs would increase during the afternoon peak temperature period. We relocated lizards three times daily for 24 days and scored whether lizards were within 0.5 m of a shrub, which we used as an indicator of shrub association. For each relocation, we also scored lizard association with a set of predefined microhabitat features. We also scored lizard behavior according to a set of predefined behavioral traits. We constructed home ranges following the minimum convex polygon method and generated estimates of shrub density and relative shrub area within each home range polygon. We obtained 1,190 datapoints from a sample of 27 lizards. We found that lizards were associated with open sites significantly more often than with shrubs but were associated with shrubs more than predicted by percent shrub area within their home ranges. Lizards were associated significantly more often under shrubs during the afternoon peak temperature period, and lizards were observed cooling under shrubs significantly more often. The frequency of association of individual lizards with shrubs was not correlated with the density of shrubs within their home range. Synthesis and Applications. Shrubs can be considered as a component of high-quality habitat for ectothermic desert vertebrates for the purposes of restoration and management. Furthermore, radiotelemetry provides a novel methodological approach for assessing shrub-animal facilitative interactions within desert communities.

Contemporary Drought and Future Effects of Climate Change on the Endangered Blunt-Nosed Leopard Lizard, Gambelia sila.

Extreme weather events can provide unique opportunities for testing models that predict the effect of climate change. Droughts of increasing severity have been predicted under numerous models, thus contemporary droughts may allow us to test these models prior to the onset of the more extreme effects predicted with a changing climate. In the third year of an ongoing severe drought, surveys failed to detect neonate endangered blunt-nosed leopard lizards in a subset of previously surveyed populations where we expected to see them. By conducting surveys at a large number of sites across the range of the species over a short time span, we were able to establish a strong positive correlation between winter precipitation and the presence of neonate leopard lizards over geographic space. Our results are consistent with those of numerous longitudinal studies and are in accordance with predictive climate change models. We suggest that scientists can take immediate advantage of droughts while they are still in progress to test patterns of occurrence in other drought-sensitive species and thus provide for more robust models of climate change effects on biodiversity.

Heritable variation in garter snake color patterns in postglacial populations.

Global climate change is expected to trigger northward shifts in the ranges of natural populations of plants and animals, with subsequent effects on intraspecific genetic diversity. Investigating how genetic diversity is patterned among populations that arose following the last Ice Age is a promising method for understanding the potential future effects of climate change. Theoretical and empirical work has suggested that overall genetic diversity can decrease in colonial populations following rapid expansion into postglacial landscapes, with potential negative effects on the ability of populations to adapt to new environmental regimes. The crucial measure of this genetic variation and a population's overall adaptability is the heritable variation in phenotypic traits, as it is this variation that mediates the rate and direction of a population's multigenerational response to selection. Using two large full-sib quantitative genetic studies (N(Manitoba) = 144; N(South Dakota) = 653) and a smaller phenotypic analysis from Kansas (N(Kansas) = 44), we compared mean levels of pigmentation, genetic variation and heritability in three pigmentation traits among populations of the common garter snake, Thamnophis sirtalis, along a north-south gradient, including a postglacial northern population and a putative southern refuge population. Counter to our expectations, we found that genetic variance and heritability for the three pigmentation traits were the same or higher in the postglacial population than in the southern population.