Sustained predation pressure may prevent the loss of anti-predator traits from havened populations.

Conservation havens free of invasive predators are increasingly relied upon for fauna conservation, although havened populations can lose anti-predator traits, likely making them less suitable for life 'beyond the fence'. Sustaining low levels of mammalian predator pressure inside havens may prevent the loss of anti-predator traits from havened populations. We opportunistically compared behavioural and morphological anti-predator traits between four woylie (Bettongia penicillata ogilbyi) populations- one haven isolated from all mammalian predators, one haven containing a native mammalian predator (chuditch; Dasyurus geoffroii), and their respective non-havened counterparts (each containing both chuditch and invasive predators). Havened woylies existing without mammalian predators were smaller (shorter hindfeet, smaller body weight) and less reactive (consumed more food from fox-treated and control feeding stations, less agitated during human handling) than a non-havened reference population. However, in the haven containing chuditch, we found no difference in behaviour or morphology compared to the adjacent non-havened population. Across populations, anti-predator responses tended to appear stronger at sites with higher predator activity, suggestive of an adaptive response across a gradient of predation pressure. Our findings suggest that maintaining mammalian predation pressure in conservation havens could be effective for preventing or slowing the loss of anti-predator traits from these populations.

Diversity and Evolution of Frog Visual Opsins: Spectral Tuning and Adaptation to Distinct Light Environments.

Visual systems adapt to different light environments through several avenues including optical changes to the eye and neurological changes in how light signals are processed and interpreted. Spectral sensitivity can evolve via changes to visual pigments housed in the retinal photoreceptors through gene duplication and loss, differential and coexpression, and sequence evolution. Frogs provide an excellent, yet understudied, system for visual evolution research due to their diversity of ecologies (including biphasic aquatic-terrestrial life cycles) that we hypothesize imposed different selective pressures leading to adaptive evolution of the visual system, notably the opsins that encode the protein component of the visual pigments responsible for the first step in visual perception. Here, we analyze the diversity and evolution of visual opsin genes from 93 new eye transcriptomes plus published data for a combined dataset spanning 122 frog species and 34 families. We find that most species express the four visual opsins previously identified in frogs but show evidence for gene loss in two lineages. Further, we present evidence of positive selection in three opsins and shifts in selective pressures associated with differences in habitat and life history, but not activity pattern. We identify substantial novel variation in the visual opsins and, using microspectrophotometry, find highly variable spectral sensitivities, expanding known ranges for all frog visual pigments. Mutations at spectral-tuning sites only partially account for this variation, suggesting that frogs have used tuning pathways that are unique among vertebrates. These results support the hypothesis of adaptive evolution in photoreceptor physiology across the frog tree of life in response to varying environmental and ecological factors and further our growing understanding of vertebrate visual evolution.

Population genomic diversity and structure in the golden bandicoot: a history of isolation, extirpation, and conservation.

Using genetic information to develop and implement conservation programs is vital for maintaining biodiversity and ecosystem resilience. Evaluation of the genetic variability within and among remnant populations can inform management of both natural and translocated populations to maximise species' adaptive potential, mitigate negative impacts of inbreeding, and subsequently minimise risk of extinction. Here we use reduced representation sequencing to undertake a genetic assessment of the golden bandicoot (Isoodon auratus), a threatened marsupial endemic to Australia. The currently recognised taxon consists of three subspecies distributed among multiple natural and translocated populations. After confirming the genetic distinctiveness of I. auratus from two closely related taxa, I. fusciventer and I. macrourus, we identified four genetic clusters within I. auratus. These clusters exhibited substantial genetic differentiation (pairwise FST values ranging from 0.18 to 0.65, pairwise DXY ranging from 0.1 to 0.168), reflecting long-term isolation of some populations on offshore islands and the influence of genetic drift. Mainland natural populations in the Kimberley region had the highest genetic diversity and the largest contribution to overall allelic and gene diversity compared to both natural and translocated island populations. A population translocated to Guluwuru Island in the Northern Territory had the lowest genetic diversity. Our data suggest that island populations can appear genetically unique due to genetic drift and this needs to be taken into account when considering genetic diversity in conservation efforts to maintain overall genetic diversity of the species. We effectively demonstrate how genomic information can guide practical conservation planning, especially when declining species are represented by multiple isolated populations.

Using PVA and captive breeding to balance trade-offs in the rescue of the island dibbler onto a new island ark.

In the face of the current global extinction crisis, it is critical we give conservation management strategies the best chance of success. Australia is not exempt from global trends with currently the world's greatest mammal extinction rate (~ 1 per 8 years). Many more are threatened including the dibbler (Parantechinus apicalis) whose remnant range has been restricted to Western Australia at just one mainland site and two small offshore islands-Whitlock Island (5 ha) and Boullanger Island (35 ha). Here, we used 14 microsatellite markers to quantify genetic variation in the remaining island populations from 2013 to 2018 and incorporated these data into population viability analysis (PVA) models, used to assess factors important to dibbler survival and to provide guidance for translocations. Remnant population genetic diversity was low (< 0.3), and populations were highly divergent from each other (pairwise FSTs 0.29-0.52). Comparison of empirical data to an earlier study is consistent with recent declines in genetic diversity and models projected increasing extinction risk and declining genetic variation in the next century. Optimal translocation scenarios recommend 80 founders for new dibbler populations-provided by captive breeding-and determined the proportion of founders from parental populations to maximise genetic diversity and minimise harvesting impact. The goal of our approach is long-term survival of genetically diverse, self-sustaining populations and our methods are transferable. We consider mixing island with mainland dibblers to reinforce genetic variation.

A global reptile assessment highlights shared conservation needs of tetrapods.

Comprehensive assessments of species' extinction risks have documented the extinction crisis1 and underpinned strategies for reducing those risks2. Global assessments reveal that, among tetrapods, 40.7% of amphibians, 25.4% of mammals and 13.6% of birds are threatened with extinction3. Because global assessments have been lacking, reptiles have been omitted from conservation-prioritization analyses that encompass other tetrapods4-7. Reptiles are unusually diverse in arid regions, suggesting that they may have different conservation needs6. Here we provide a comprehensive extinction-risk assessment of reptiles and show that at least 1,829 out of 10,196 species (21.1%) are threatened-confirming a previous extrapolation8 and representing 15.6 billion years of phylogenetic diversity. Reptiles are threatened by the same major factors that threaten other tetrapods-agriculture, logging, urban development and invasive species-although the threat posed by climate change remains uncertain. Reptiles inhabiting forests, where these threats are strongest, are more threatened than those in arid habitats, contrary to our prediction. Birds, mammals and amphibians are unexpectedly good surrogates for the conservation of reptiles, although threatened reptiles with the smallest ranges tend to be isolated from other threatened tetrapods. Although some reptiles-including most species of crocodiles and turtles-require urgent, targeted action to prevent extinctions, efforts to protect other tetrapods, such as habitat preservation and control of trade and invasive species, will probably also benefit many reptiles.

Fitness consequences of targeted gene flow to counter impacts of drying climates on terrestrial-breeding frogs.

Targeted gene flow (TGF) could bolster the adaptive potential of isolated populations threatened by climate change, but could also lead to outbreeding depression. Here, we explore these possibilities by creating mixed- and within-population crosses in a terrestrial-breeding frog species threatened by a drying climate. We reared embryos of the crawling frog (Pseudophryne guentheri) on wet and dry soils and quantified fitness-related traits upon hatching. TGF produced mixed outcomes in hybrids, which depended on crossing direction (origin of gametes from each sex). North-south crosses led to low embryonic survival if eggs were of a southern origin, and high malformation rates when eggs were from a northern population. Conversely, east-west crosses led to one instance of hybrid vigour, evident by increased fitness and desiccation tolerance of hybrid offspring relative to offspring produced from within-population crosses. These contrasting results highlight the need to experimentally evaluate the outcomes of TGF for focal species across generations prior to implementing management actions.

Low desiccation and thermal tolerance constrains a terrestrial amphibian to a rare and disappearing microclimate niche.

Drier and hotter conditions caused by climate change threaten species that exist close to their physiological limits, as well as those with limited ability to move. Habitat specialists may also be particularly vulnerable if they have specific abiotic requirements. Here we assess whether thermal and hydric constraints can explain the highly restricted and declining distributions of the critically endangered terrestrial-breeding frog, Geocrinia alba. We also evaluate the species' vulnerability to climate change based on the similarity of current microclimatic conditions to their physiological limits. We found that G. alba had low thresholds of thermal and desiccation tolerance relative to other anuran species. The estimated thermal optimum (Topt ) and critical thermal maxima (CTmax ) were 23.3°C and 29.6°C, respectively, and adult frogs had an absorption threshold (AT, the lowest water potential at which water can be absorbed from a substrate) of -50 kPa, the lowest recorded for an amphibian. Comparing environmental conditions and water loss in the field using agar models showed that riparian habitats where frogs occur provide a unique microclimate in the landscape, offering significantly lower desiccation risk during extreme summer conditions compared to immediately adjacent riparian and terrestrial habitats. Monitoring of microclimate conditions within occupied frog habitats over 2 years showed that in extreme dry and hot years the AT was exceeded at six of eight sites, and Topt was exceeded at two of eight sites. Given their specific physiological limits, the apparent rarity of suitable microclimates and a regional drying-warming trend, we suggest that G. alba occupies a potentially disappearing niche and may be indicative of other habitat specialists that rely on ephemeral drainages. More broadly, this study highlights that desiccation thresholds may tightly constrain amphibian distributions and need to be considered along with thermal tolerance thresholds when predicting the impacts of climate change.

Extensive geographical variation in testes size and ejaculate traits in a terrestrial-breeding frog.

Ejaculate traits vary extensively among individuals and species, but little is known about their variation among populations of the same species. Here, we investigated patterns of intraspecific variation in male reproductive investment in the terrestrial-breeding frog Pseudophryne guentheri. Like most anurans, breeding activity in P. guentheri is cued by precipitation, and therefore the timing and duration of breeding seasons differ among geographically separated populations, potentially leading to differences in the level of sperm competition. We, therefore, anticipated local adaptation in sperm traits that reflect these phenological differences among populations. Our analysis of six natural populations across a rainfall gradient revealed significant divergence in testes and ejaculate traits that correspond with annual rainfall and rainfall seasonality; males from the northern and drier edge of the species range had significantly smaller testes containing fewer, smaller and less motile sperm compared with those from mesic central populations. These findings may reflect spatial variation in the strength of postcopulatory sexual selection, likely driven by local patterns of precipitation.

Microclimate modelling of beach sand temperatures reveals high spatial and temporal variation at sea turtle rookeries.

The continual development of ecological models and availability of high-resolution gridded climate surfaces have stimulated studies that link climate variables to functional traits of organisms. A primary constraint of these studies is the ability to reliably predict the microclimate that an organism experiences using macroscale climate inputs. This is particularly important in regions where access to empirical information is limited. Here, we contrast correlative models based on both ambient and sea surface temperatures to mechanistic modelling approaches to predict beach sand temperatures at depths relevant to sea turtle nesting. We show that mechanistic models are congruent with correlative models at predicting sand temperatures. We used these predictions to explore thermal variation across 46 mainland and island beaches that span the geographical range of sea turtle nesting in Western Australia. Using high resolution gridded climate surfaces and site-specific soil reflectance, we predict almost 9 °C variation in average annual temperatures between beaches, and nearly 10 °C variation in average temperatures during turtle nesting seasons. Validation of models demonstrated that predictions were typically within 2 °C of observations and, although most sites had high correlations (r2 > 0.7), predictive capacity varied between sites. An advantage of the mechanistic model demonstrated here is that it can be used to explore the impacts of climate change on sea turtle nesting beach temperatures as, unlike correlative models, it can be forced with novel combinations of environmental variables.

A genome-wide search for local adaptation in a terrestrial-breeding frog reveals vulnerability to climate change.

Terrestrial-breeding amphibians are likely to be vulnerable to warming and drying climates, as their embryos require consistent moisture for successful development. Adaptation to environmental change will depend on sufficient genetic variation existing within or between connected populations. Here, we use Single Nucleotide Polymorphism (SNP) data to investigate genome-wide patterns in genetic diversity, gene flow and local adaptation in a terrestrial-breeding frog (Pseudophryne guentheri) subject to a rapidly drying climate and recent habitat fragmentation. The species was sampled across 12 central and range-edge populations (192 samples), and strong genetic structure was apparent, as were high inbreeding coefficients. Populations showed differences in genetic diversity, and one population lost significant genetic diversity in a decade. More than 500 SNP loci were putatively under directional selection, and 413 of these loci were correlated with environmental variables such as temperature, rainfall, evaporation and soil moisture. One locus showed homology to a gene involved in the activation of maturation in Xenopus oocytes, which may facilitate rapid development of embryos in drier climates. The low genetic diversity, strong population structuring and presence of local adaptation revealed in this study shows why management strategies such as targeted gene flow may be necessary to assist isolated populations to adapt to future climates.

The Influence of Temperature on Embryonic Respiration, Growth, and Sex Determination in a Western Australian Population of Green Turtles (Chelonia mydas).

The thermal environment of sea turtle embryos has marked effects on many aspects of their development and energetics and has consequences for posthatching stages. Here we incubated Chelonia mydas embryos from Ningaloo Reef in Western Australia at a range of temperatures (27°, 29°, 30°, 31°, 32°, and 30° ± 5°C) to determine development rates and the pivotal temperature for sex determination. We also measured embryonic growth, oxygen consumption, and carbon dioxide production throughout development at 27° and 31°C. Metabolic rates were higher at 31°C than at 27°C, but total energy expenditure was greater at 27°C, with 2,281 mL of oxygen consumed compared with 1,992 mL at 31°C. Respiration at both temperatures showed a pattern typical of sea turtle embryos, with peak rates occurring at approximately 85% of development and then declining toward hatching. Hatchlings produced at higher incubation temperatures developed faster, were smaller, and had larger residual yolk masses than hatchlings produced at lower temperatures. The pivotal temperature that produced an equal sex ratio was 29.2°C, with mixed sexes produced between 27.9° and 30.4°C. Our results showed that the Ningaloo population of C. mydas has somewhat different thermal sensitivities than other C. mydas populations and justified why is it necessary to collect population-specific data to accurately project the impacts of global warming on focal populations.

Environmental Stress Increases the Magnitude of Nonadditive Genetic Variation in Offspring Fitness in the Frog Crinia georgiana.

When organisms encounter heterogeneous environments, selection may favor the ability of individuals to tailor their phenotypes to suit the prevailing conditions. Understanding the genetic basis of plastic responses is therefore vital for predicting whether susceptible populations can adapt and persist under new selection pressures. Here, we investigated whether there is potential for adaptive plasticity in development time in the quacking frog Crinia georgiana, a species experiencing a drying climate. Using a North Carolina II breeding design, we exposed 90 family groups to two water depth treatments (baseline and low water) late in larval development. We then estimated the contribution of additive and nonadditive sources of genetic variation to early offspring fitness under both environments. Our results revealed a marked decline in larval fitness under the stressful (low water) rearing environment but also that additive genetic variation was negligible for all traits. However, in most cases, we found significant sire-by-dam interactions, indicating the importance of nonadditive genetic variation for offspring fitness. Moreover, sire-by-dam interactions were modified by the treatment, indicating that patterns of nonadditive genetic variance depend on environmental context. For all traits, we found higher levels of nonadditive genetic variation (relative to total phenotypic variation) when larvae were reared under stressful conditions, suggesting that the fitness costs associated with incompatible parental crosses (e.g., homozygous deleterious recessive alleles) will only be expressed when water availability is low. Taken together, our results highlight the need to consider patterns of nonadditive genetic variation under contrasting selective regimes when considering the resilience of species to environmental change.

Biodiversity redistribution under climate change: Impacts on ecosystems and human well-being.

Distributions of Earth's species are changing at accelerating rates, increasingly driven by human-mediated climate change. Such changes are already altering the composition of ecological communities, but beyond conservation of natural systems, how and why does this matter? We review evidence that climate-driven species redistribution at regional to global scales affects ecosystem functioning, human well-being, and the dynamics of climate change itself. Production of natural resources required for food security, patterns of disease transmission, and processes of carbon sequestration are all altered by changes in species distribution. Consideration of these effects of biodiversity redistribution is critical yet lacking in most mitigation and adaptation strategies, including the United Nation's Sustainable Development Goals.

Sex ratio bias and extinction risk in an isolated population of Tuatara (Sphenodon punctatus).

Understanding the mechanisms underlying population declines is critical for preventing the extinction of endangered populations. Positive feedbacks can hasten the process of collapse and create an 'extinction vortex,' particularly in small, isolated populations. We provide a case study of a male-biased sex ratio creating the conditions for extinction in a natural population of tuatara (Sphenodon punctatus) on North Brother Island in the Cook Strait of New Zealand. We combine data from long term mark-recapture surveys, updated model estimates of hatchling sex ratio, and population viability modeling to measure the impacts of sex ratio skew. Results from the mark-recapture surveys show an increasing decline in the percentage of females in the adult tuatara population. Our monitoring reveals compounding impacts on female fitness through reductions in female body condition, fecundity, and survival as the male-bias in the population has increased. Additionally, we find that current nest temperatures are likely to result in more male than female hatchlings, owing to the pattern of temperature-dependent sex determination in tuatara where males hatch at warmer temperatures. Anthropogenic climate change worsens the situation for this isolated population, as projected temperature increases for New Zealand are expected to further skew the hatchling sex ratio towards males. Population viability models predict that without management intervention or an evolutionary response, the population will ultimately become entirely comprised of males and functionally extinct. Our study demonstrates that sex ratio bias can be an underappreciated threat to population viability, particularly in populations of long-lived organisms that appear numerically stable.

Detecting extinction risk from climate change by IUCN Red List criteria.

Anthropogenic climate change is a key threat to global biodiversity. To inform strategic actions aimed at conserving biodiversity as climate changes, conservation planners need early warning of the risks faced by different species. The IUCN Red List criteria for threatened species are widely acknowledged as useful risk assessment tools for informing conservation under constraints imposed by limited data. However, doubts have been expressed about the ability of the criteria to detect risks imposed by potentially slow-acting threats such as climate change, particularly because criteria addressing rates of population decline are assessed over time scales as short as 10 years. We used spatially explicit stochastic population models and dynamic species distribution models projected to future climates to determine how long before extinction a species would become eligible for listing as threatened based on the IUCN Red List criteria. We focused on a short-lived frog species (Assa darlingtoni) chosen specifically to represent potential weaknesses in the criteria to allow detailed consideration of the analytical issues and to develop an approach for wider application. The criteria were more sensitive to climate change than previously anticipated; lead times between initial listing in a threatened category and predicted extinction varied from 40 to 80 years, depending on data availability. We attributed this sensitivity primarily to the ensemble properties of the criteria that assess contrasting symptoms of extinction risk. Nevertheless, we recommend the robustness of the criteria warrants further investigation across species with contrasting life histories and patterns of decline. The adequacy of these lead times for early warning depends on practicalities of environmental policy and management, bureaucratic or political inertia, and the anticipated species response times to management actions.

How to decide whether to move species threatened by climate change.

Introducing species to areas outside their historical range to secure their future under climate change is a controversial strategy for preventing extinction. While the debate over the wisdom of this strategy continues, such introductions are already taking place. Previous frameworks for analysing the decision to introduce have lacked a quantifiable management objective and mathematically rigorous problem formulation. Here we develop the first rigorous quantitative framework for deciding whether or not a particular introduction should go ahead, which species to prioritize for introduction, and where and how to introduce them. It can also be used to compare introduction with alternative management actions, and to prioritise questions for future research. We apply the framework to a case study of tuatara (Sphenodon punctatus) in New Zealand. While simple and accessible, this framework can accommodate uncertainty in predictions and values. It provides essential support for the existing IUCN guidelines by presenting a quantitative process for better decision-making about conservation introductions.

Patterns of genetic variation in desiccation tolerance in embryos of the terrestrial-breeding frog, Pseudophryne guentheri.

Environmental change often requires evolutionary responses, and therefore understanding the genetic architecture of susceptible populations is essential for predicting their capacity to respond adaptively. However, quantitative genetic studies are rarely targeted at populations considered vulnerable to such environmental perturbations. Here, we assess the level of heritable variation in the ability of embryos to tolerate desiccation stress in Pseudophryne guentheri, a terrestrial-breeding frog that is currently experiencing a drying climate. We applied a North Carolina II breeding design to identify sources of genetic and environmental variance, and genotype-by-environment interactions (GEIs), underlying the expression of embryo survival, hatching times, hatchling mass, size, and shape. Our analysis revealed highly significant effects of water potential and maternal effects on all measured traits, while additive genetic effects were significant for hatchling shape, and nonadditive effects were observed for embryo survival. Interestingly, GEIs, including for some traits complex three-way sire-by-dam-by-environment interactions, were significant, indicating that progeny from certain male-female crosses were more tolerant to water stress than others. These findings suggest a limited capacity of P. guentheri to respond to a drying climate, but also reveal that the detrimental effects of nonviable male-female crosses (i.e., genetic incompatibility) can be masked in benign environments.

Securing the demographic and genetic future of tuatara through assisted colonization.

Climate change poses a particular threat to species with fragmented distributions and little or no capacity to migrate. Assisted colonization, moving species into regions where they have not previously occurred, aims to establish populations where they are expected to survive as climatic envelopes shift. However, adaptation to the source environment may affect whether species successfully establish in new regions. Assisted colonization has spurred debate among conservation biologists and ecologists over whether the potential benefits to the threatened species outweigh the potential disruption to recipient communities. In our opinion, the debate has been distracted by controversial examples, rather than cases where assisted colonization may be a viable strategy. We present a strategic plan for the assisted migration of tuatara (Sphenodon punctatus), an endemic New Zealand reptile. The plan includes use of extant populations as reference points for comparisons with assisted-colonization populations with respect to demography, phenotypic plasticity, and phenology; optimization of genetic variation; research to fill knowledge gaps; consideration of host and recipient communities; and inclusion of stakeholders in the planning stage. When strategically planned and monitored, assisted colonization could meet conservation and research goals and ultimately result in the establishment of long-term sustainable populations capable of persisting during rapid changes in climate.

Does incubation temperature fluctuation influence hatchling phenotypes in reptiles? A test using parthenogenetic geckos.

Many lineages of parthenogenetic organisms have persisted through significant environmental change despite the constraints imposed by their fixed genotype and limited evolutionary potential. The ability of parthenogens to occur sympatrically with sexual relatives may in part be due to phenotypic plasticity in their responses to their environment, especially with respect to incubation temperature--a maternally selected trait. Here we measured the incubation temperatures selected by two lineages of triploid parthenogenic geckos in the Heteronotia binoei complex by allowing them to deposit clutches along a thermal gradient. The average nest temperature selected was 28.4 degrees C, with no significant differences between parthenogenic races or individual clones. To investigate the effect of nest-temperature variability on physiological and morphological traits, we incubated eggs from different races at one of four incubation regimes (32 degrees +/- 0 degrees, +/- 3 degrees , +/- 5 degrees , or +/- 9 degrees C). Embryos incubated at constant 32 degrees C developed faster than embryos reared under increasing extremes of diel temperature fluctuation (+/- 3 degrees , +/- 5 degrees C), and incubation at 32 degrees +/- 9 degrees C was unsuccessful. Incubation regime had no effect on the body size, preferred substrate temperature, or mass-specific .V(O2) of hatchlings. However, parthenogenic race had a significant effect on egg mass, tail length, snout-to-vent length, total length, and .V(O2) . We conclude that developmental traits are strongly influenced by clonal genotypes in this parthenogenic complex but are well buffered against fluctuations in incubation temperature.

Phenotypic differences in terrestrial frog embryos: effect of water potential and phase.

The terrestrial embryos of many amphibians obtain water in two ways; in a liquid phase from the substrate on which eggs are deposited, and in a vapour phase from the surrounding atmosphere. We tested whether the mode of water flux (liquid or vapour) affected the morphology and metabolic traits of the terrestrial Victorian smooth froglet (Geocrinia victoriana) embryos by incubating eggs both with a liquid water source and at a range of vapour water potentials. We found that embryos incubated with a liquid water source (psi(pi)=0 kPa) were better hydrated than embryos incubated with a vapour water source (psi(v)=0 kPa), and grew to a larger size. Eggs incubated in atmospheres with lower psi(v) values showed significant declines in mass and in the thickness of the jelly capsule, while embryos primarily showed reductions in dry mass, total length, tail length and fin height. The most significant deviations from control (psi(v)=0 kPa) values were observed when the psi(v) of the incubation media was less than the osmotic water potential (psi(pi)) of the embryonic interstitial fluid (approximately -425 kPa). Despite the caveat that a psi(v) of 0 kPa is probably difficult to achieve under our experimental conditions, the findings indicate the importance for eggs under natural conditions of contacting liquid water in the nesting substrate to allow swelling of the capsule.