Constant-temperature predictions underestimate growth of a fungal amphibian pathogen under individual host thermal profiles.

Ectotherm body temperatures fluctuate with environmental variability and host behavior, which may influence host-pathogen interactions. Fungal pathogens are a major threat to ectotherms and may be highly responsive to the fluctuating thermal profiles of individual hosts, especially cool-loving fungi exposed to high host temperatures. However, most studies estimate pathogen thermal performance based on averages of host or surrogate environmental temperatures, potentially missing effects of short-term host temperature shifts such as daily or hourly heat spikes. We recorded individual thermal profiles of Australian rainforest frogs using temperature-sensitive radio-transmitters. We then reproduced a subset of individual thermal profiles in growth chambers containing cultures of the near-global amphibian pathogen Batrachochytrium dendrobatidis (Bd) to investigate how realistic host temperature profiles affect Bd growth. We focused on thermal profiles that exceed the thermal optimum of Bd because the effects of realistic heat spikes on Bd growth are unresolved. Our laboratory incubation experiment revealed that Bd growth varied in response to relatively small differences in heat spike characteristics of individual frog thermal profiles, such as a single degree or a few hours, highlighting the importance of individual host behaviors in predicting population-level disease dynamics. The fungus also grew better than predicted under the most extreme and unpredictable frog temperature profile, recovering from two days of extreme (nearly 32 °C) heat spikes without negative effects on overall growth, suggesting we are underestimating the growth potential of the pathogen in nature. Combined with the previous finding that Bd reduces host heat tolerance, our study suggests that this pathogen may carry a competitive edge over hosts in the face of anthropogenic climate change.

Predicting the growth of the amphibian chytrid fungus in varying temperature environments.

Environmental temperature is a crucial abiotic factor that influences the success of ectothermic organisms, including hosts and pathogens in disease systems. One example is the amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd), which has led to widespread amphibian population declines. Understanding its thermal ecology is essential to effectively predict outbreaks. Studies that examine the impact of temperature on hosts and pathogens often do so in controlled constant temperatures. Although varying temperature experiments are becoming increasingly common, it is unrealistic to test every temperature scenario. Thus, reliable methods that use constant temperature data to predict performance in varying temperatures are needed. In this study, we tested whether we could accurately predict Bd growth in three varying temperature regimes, using a Bayesian hierarchical model fit with constant temperature Bd growth data. We fit the Bayesian hierarchical model five times, each time changing the thermal performance curve (TPC) used to constrain the logistic growth rate to determine how TPCs influence the predictions. We then validated the model predictions using Bd growth data collected from the three tested varying temperature regimes. Although all TPCs overpredicted Bd growth in the varying temperature regimes, some functional forms performed better than others. Varying temperature impacts on disease systems are still not well understood and improving our understanding and methodologies to predict these effects could provide insights into disease systems and help conservation efforts.

Host thermoregulatory constraints predict growth of an amphibian chytrid pathogen (Batrachochytrium dendrobatidis).

1. The course and outcome of many wildlife diseases are context-dependent, and therefore change depending on the behaviour of hosts and environmental response of the pathogen. 2. Contemporary declines in amphibian populations are widely attributed to chytridiomycosis, caused by the pathogenic fungus Batrachochytrium dendrobatidis. Despite the thermal sensitivity of the pathogen and its amphibian hosts, we do not understand how host thermal regimes experienced by frogs in the wild directly influence pathogen growth. 3. We tested how thermal regimes experienced by the rainforest frog Litoria rheocola in the wild influence pathogen growth in the laboratory, and whether these responses differ from pathogen growth under available environmental thermal regimes. 4. Frog thermal regimes mimicked in the laboratory accelerated pathogen growth during conditions representative of winter at high elevations more so than if temperatures matched air or stream water temperatures. By contrast, winter frog thermal regimes at low elevations slowed pathogen growth relative to air temperatures, but not water temperatures. 5. The growth pattern of the fungus under frog thermal regimes matches field prevalence and intensity of infections for this species (high elevation winter > high elevation summer > low elevation winter > low elevation summer), whereas pathogen growth trajectories under environmental temperatures did not match these patterns. 6. If these laboratory results translate into field responses, tropical frogs may be able to reduce disease impacts by regulating their body temperatures to limit pathogen growth (e.g., by using microhabitats that facilitate basking to reach high temperatures); in other cases, the environment may limit the ability of frogs to thermoregulate such that individuals are more vulnerable to this pathogen (e.g., in dense forests at high elevations). 7. Species-specific thermoregulatory behaviour, and interactions with and constraints imposed by the environment, are therefore essential to understanding and predicting the spatial and temporal impacts of this global disease.

When males live longer: Resource-driven territorial behavior drives sex-specific survival in snakes.

Phylogenetic analysis has shown that males' propensity to engage in aggressive encounters is associated with females having greater longevity. Here, we confirm the causal link between aggression and reduced longevity by looking at an egg-eating snake (Oligodon formosanus) in which females defend territories in the presence of sea turtle eggs. We monitored aggressiveness and survival at two sites: a control site with a stable supply of turtle eggs, and a second site where we collected data before and after a storm that eroded the beach on which turtles nested, thus leading to a loss of territoriality. We show that territoriality was the driver behind higher injury rates in females. Territorial females also had lower survival and decreased longevity compared with the nonterritorial males, but these differences disappeared when females were not territorial. Our study demonstrates how resource availability can influence the evolution of sex-specific patterns of survival across vertebrates.

Infection increases vulnerability to climate change via effects on host thermal tolerance.

Unprecedented global climate change and increasing rates of infectious disease emergence are occurring simultaneously. Infection with emerging pathogens may alter the thermal thresholds of hosts. However, the effects of fungal infection on host thermal limits have not been examined. Moreover, the influence of infections on the heat tolerance of hosts has rarely been investigated within the context of realistic thermal acclimation regimes and potential anthropogenic climate change. We tested for effects of fungal infection on host thermal tolerance in a model system: frogs infected with the chytrid Batrachochytrium dendrobatidis. Infection reduced the critical thermal maxima (CTmax) of hosts by up to ~4 °C. Acclimation to realistic daily heat pulses enhanced thermal tolerance among infected individuals, but the magnitude of the parasitism effect usually exceeded the magnitude of the acclimation effect. In ectotherms, behaviors that elevate body temperature may decrease parasite performance or increase immune function, thereby reducing infection risk or the intensity of existing infections. However, increased heat sensitivity from infections may discourage these protective behaviors, even at temperatures below critical maxima, tipping the balance in favor of the parasite. We conclude that infectious disease could lead to increased uncertainty in estimates of species' vulnerability to climate change.

Climate change and nesting behaviour in vertebrates: a review of the ecological threats and potential for adaptive responses.

Nest building is a taxonomically widespread and diverse trait that allows animals to alter local environments to create optimal conditions for offspring development. However, there is growing evidence that climate change is adversely affecting nest-building in animals directly, for example via sea-level rises that flood nests, reduced availability of building materials, and suboptimal sex allocation in species exhibiting temperature-dependent sex determination. Climate change is also affecting nesting species indirectly, via range shifts into suboptimal nesting areas, reduced quality of nest-building environments, and changes in interactions with nest predators and parasites. The ability of animals to adapt to sustained and rapid environmental change is crucial for the long-term persistence of many species. Many animals are known to be capable of adjusting nesting behaviour adaptively across environmental gradients and in line with seasonal changes, and this existing plasticity potentially facilitates adaptation to anthropogenic climate change. However, whilst alterations in nesting phenology, site selection and design may facilitate short-term adaptations, the ability of nest-building animals to adapt over longer timescales is likely to be influenced by the heritable basis of such behaviour. We urgently need to understand how the behaviour and ecology of nest-building in animals is affected by climate change, and particularly how altered patterns of nesting behaviour affect individual fitness and population persistence. We begin our review by summarising how predictable variation in environmental conditions influences nest-building animals, before highlighting the ecological threats facing nest-building animals experiencing anthropogenic climate change and examining the potential for changes in nest location and/or design to provide adaptive short- and long-term responses to changing environmental conditions. We end by identifying areas that we believe warrant the most urgent attention for further research.

Robust calling performance in frogs infected by a deadly fungal pathogen.

Reproduction is an energetically costly behavior for many organisms, including species with mating systems in which males call to attract females. In these species, calling males can often attract more females by displaying more often, with higher intensity, or at certain frequencies. Male frogs attract females almost exclusively by calling, and we know little about how pathogens, including the globally devastating fungus, Batrachochytrium dendrobatidis, influence calling effort and call traits. A previous study demonstrated that the nightly probability of calling by male treefrogs, Litoria rheocola, is elevated when they are in good body condition and are infected by B. dendrobatidis. This suggests that infections may cause males to increase their present investment in mate attraction to compensate for potential decreases in future reproduction. However, if infection by B. dendrobatidis decreases the attractiveness of their calls, infected males might experience decreased reproductive success despite increases in calling effort. We examined whether calls emitted by L. rheocola infected by B. dendrobatidis differed from those of uninfected individuals in duration, pulse rate, dominant frequency, call rate, or intercall interval, the attributes commonly linked to mate choice. We found no effects of fungal infection status or infection intensity on any call attribute. Our results indicate that infected males produce calls similar in all the qualities we measured to those of uninfected males. It is therefore likely that the calls of infected and uninfected males should be equally attractive to females. The increased nightly probability of calling previously demonstrated for infected males in good condition may therefore lead to greater reproductive success than that of uninfected males. This could reduce the effectiveness of natural selection for resistance to infection, but could increase the effectiveness of selection for infection tolerance, the ability to limit the harm caused by infection, such as reductions in body condition.

Surf and turf: predation by egg-eating snakes has led to the evolution of parental care in a terrestrial lizard.

Animals display a great diversity of parental care tactics that ultimately enhance offspring survival, but how such behaviors evolve remains unknown for most systems. Here, we studied the evolution of maternal care, in the form of nest guarding, in a single population of long-tailed sun skink (Eutropis longicaudata) living on Orchid Island (Taiwan). This species typically does not provide protection to its offspring. Using a common garden experiment, we show that maternal care is genetically determined in this population. Through field manipulations, we demonstrate that care provides a significant increase in egg survival on Orchid Island by reducing predation from egg-eating snakes (Oligodon formosanus); this predator is not abundant in other populations of the lizard, which do not display parental care. Finally, using extensive field surveys, we show that the seasonal availability of green sea turtle (Chelonia mydas) nests is the cause for the high abundance of snake predators on Orchid Island, with the snakes consuming lizard eggs when green turtle eggs are not available. Together, these lines of evidence provide the first full demonstration of how predation can trigger the evolution of parental care in a species derived from a non-caring ancestor.

Nest inundation from sea-level rise threatens sea turtle population viability.

Contemporary sea-level rise will inundate coastal habitats with seawater more frequently, disrupting the life cycles of terrestrial fauna well before permanent habitat loss occurs. Sea turtles are reliant on low-lying coastal habitats worldwide for nesting, where eggs buried in the sand remain vulnerable to inundation until hatching. We show that saltwater inundation directly lowers the viability of green turtle eggs (Chelonia mydas) collected from the world's largest green turtle nesting rookery at Raine Island, Australia, which is undergoing enigmatic decline. Inundation for 1 or 3 h reduced egg viability by less than 10%, whereas inundation for 6 h reduced viability by approximately 30%. All embryonic developmental stages were vulnerable to mortality from saltwater inundation. Although the hatchlings that emerged from inundated eggs displayed normal physical and behavioural traits, hypoxia during incubation could influence other aspects of the physiology or behaviour of developing embryos, such as learning or spatial orientation. Saltwater inundation can directly lower hatching success, but it does not completely explain the consistently low rates of hatchling production observed on Raine Island. More frequent nest inundation associated with sea-level rise will increase variability in sea turtle hatching success spatially and temporally, due to direct and indirect impacts of saltwater inundation on developing embryos.

Tropical flatback turtle (Natator depressus) embryos are resilient to the heat of climate change.

Climate change is threatening reproduction of many ectotherms by increasing nest temperatures, potentially making it more difficult for females to locate nest sites that provide suitable incubation regimes during embryonic development. Elevated nest temperatures could increase the incidence of embryonic mortality and/or maladaptive phenotypes. We investigated whether elevated nest temperatures reduce hatching success in tropical flatback turtles (Natator depressus) nesting in the Gulf of Carpentaria, Australia. Egg incubation treatments began at 29.5°C and progressively increased in temperature throughout incubation, up to maxima of 31, 32, 33, 34 and 35°C. Elevated nest temperatures did not reduce hatching success or hatchling body size relative to control temperatures (29.5°C), but did speed up embryonic development. A combination of sudden exposure to high temperatures during the first 2 weeks of incubation (>36°C for 48 h) and prolonged warming throughout incubation (from 29.5-35°C) did not reduce hatching success. We also recorded an unusually high pivotal sex-determining temperature in this flatback turtle population relative to other sea turtle populations: an equal ratio of male and female hatchlings is produced at ∼30.4°C. This adaptation may allow some flatback turtle populations to continue producing large numbers of hatchlings of both sexes under the most extreme climate change scenarios. Some tropical populations of nesting flatbacks may possess important adaptations to high-temperature incubation environments, which are not found in more southerly temperate populations.

Natural disturbance reduces disease risk in endangered rainforest frog populations.

Natural disturbances can drive disease dynamics in animal populations by altering the microclimates experienced by hosts and their pathogens. Many pathogens are highly sensitive to temperature and moisture, and therefore small changes in habitat structure can alter the microclimate in ways that increase or decrease infection prevalence and intensity in host populations. Here we show that a reduction of rainforest canopy cover caused by a severe tropical cyclone decreased the risk of endangered rainforest frogs (Litoria rheocola) becoming infected by a fungal pathogen (Batrachochytrium dendrobatidis). Reductions in canopy cover increased the temperatures and rates of evaporative water loss in frog microhabitats, which reduced B. dendrobatidis infection risk in frogs by an average of 11-28% in cyclone-damaged areas, relative to unaffected areas. Natural disturbances to the rainforest canopy can therefore provide an immediate benefit to frogs by altering the microclimate in ways that reduce infection risk. This could increase host survival and reduce the probability of epidemic disease outbreaks. For amphibian populations under immediate threat from this pathogen, targeted manipulation of canopy cover could increase the availability of warmer, drier microclimates and therefore tip the balance from host extinction to coexistence.

Condition-dependent reproductive effort in frogs infected by a widespread pathogen.

To minimize the negative effects of an infection on fitness, hosts can respond adaptively by altering their reproductive effort or by adjusting their timing of reproduction. We studied effects of the pathogenic fungus Batrachochytrium dendrobatidis on the probability of calling in a stream-breeding rainforest frog (Litoria rheocola). In uninfected frogs, calling probability was relatively constant across seasons and body conditions, but in infected frogs, calling probability differed among seasons (lowest in winter, highest in summer) and was strongly and positively related to body condition. Infected frogs in poor condition were up to 40% less likely to call than uninfected frogs, whereas infected frogs in good condition were up to 30% more likely to call than uninfected frogs. Our results suggest that frogs employed a pre-existing, plastic, life-history strategy in response to infection, which may have complex evolutionary implications. If infected males in good condition reproduce at rates equal to or greater than those of uninfected males, selection on factors affecting disease susceptibility may be minimal. However, because reproductive effort in infected males is positively related to body condition, there may be selection on mechanisms that limit the negative effects of infections on hosts.

Host-specific thermal profiles affect fitness of a widespread pathogen.

Host behavior can interact with environmental context to influence outcomes of pathogen exposure and the impact of disease on species and populations. Determining whether the thermal behaviors of individual species influence susceptibility to disease can help enhance our ability to explain and predict how and when disease outbreaks are likely to occur. The widespread disease chytridiomycosis (caused by the fungal pathogen Batrachochytrium dendrobatidis, Bd) often has species-specific impacts on amphibian communities; some host species are asymptomatic, whereas others experience mass mortalities and population extirpation. We determined whether the average natural thermal regimes experienced by sympatric frog species in nature, in and of themselves, can account for differences in vulnerability to disease. We did this by growing Bd under temperatures mimicking those experienced by frogs in the wild. At low and high elevations, the rainforest frogs Litoria nannotis, L. rheocola, and L. serrata maintained mean thermal regimes within the optimal range for pathogen growth (15-25°C). Thermal regimes for L. serrata, which has recovered from Bd-related declines, resulted in slower pathogen growth than the cooler and less variable thermal regimes for the other two species, which have experienced more long-lasting declines. For L. rheocola and L. serrata, pathogen growth was faster in thermal regimes corresponding to high elevations than in those corresponding to low elevations, where temperatures were warmer. For L. nannotis, which prefers moist and thermally stable microenvironments, pathogen growth was fastest for low-elevation thermal regimes. All of the thermal regimes we tested resulted in pathogen growth rates equivalent to, or significantly faster than, rates expected from constant-temperature experiments. The effects of host body temperature on Bd can explain many of the broad ecological patterns of population declines in our focal species, via direct effects on pathogen fitness. Understanding the functional response of pathogens to conditions experienced by the host is important for determining the ecological drivers of disease outbreaks.

The functional significance of aposematic signals: geographic variation in the responses of widespread lizard predators to colourful invertebrate prey.

Conspicuous colouration can evolve as a primary defence mechanism that advertises unprofitability and discourages predatory attacks. Geographic overlap is a primary determinant of whether individual predators encounter, and thus learn to avoid, such aposematic prey. We experimentally tested whether the conspicuous colouration displayed by Old World pachyrhynchid weevils (Pachyrhynchus tobafolius and Kashotonus multipunctatus) deters predation by visual predators (Swinhoe's tree lizard; Agamidae, Japalura swinhonis). During staged encounters, sympatric lizards attacked weevils without conspicuous patterns at higher rates than weevils with intact conspicuous patterns, whereas allopatric lizards attacked weevils with intact patterns at higher rates than sympatric lizards. Sympatric lizards also attacked masked weevils at lower rates, suggesting that other attributes of the weevils (size/shape/smell) also facilitate recognition. Allopatric lizards rapidly learned to avoid weevils after only a single encounter, and maintained aversive behaviours for more than three weeks. The imperfect ability of visual predators to recognize potential prey as unpalatable, both in the presence and absence of the aposematic signal, may help explain how diverse forms of mimicry exploit the predator's visual system to deter predation.

Embryonic oxygen enhances learning ability in hatchling lizards.

INTRODUCTION: Producing smart offspring is an important fitness trait; individuals with enhanced cognitive ability should be more adept at responding to complex environmental demands. Cognitive ability can be influenced by conditions experienced during embryonic development. Although oxygen is necessary for embryonic development, availability can be limited within the nest environment because of substrate type, hydric conditions, and temperature. We do not yet understand, however, whether oxygen availability during embryonic development influences offspring fitness, especially cognitive ability. To address this question we incubated Mongolian Racerunner lizard (Eremias argus) eggs under hypoxic (12% O2), normoxic (21% O2), and hyperoxic conditions (30% O2). RESULTS: Hypoxia not only slowed hatching time, but also resulted in constrained cognitive ability relative to hatchlings experiencing normoxic or hyperoxic incubation conditions. Oxygen did not influence hatching success, body size or sprint speed of hatchlings. CONCLUSIONS: Oxygen availability during embryonic development has important influences on incubation duration and cognitive ability of hatchling lizards. This study provides the first evidence that oxygen availability during embryonic development can modify cognitive ability of oviparous reptiles.

Forecasting the viability of sea turtle eggs in a warming world.

Animals living in tropical regions may be at increased risk from climate change because current temperatures at these locations already approach critical physiological thresholds. Relatively small temperature increases could cause animals to exceed these thresholds more often, resulting in substantial fitness costs or even death. Oviparous species could be especially vulnerable because the maximum thermal tolerances of incubating embryos is often lower than adult counterparts, and in many species mothers abandon the eggs after oviposition, rendering them immobile and thus unable to avoid extreme temperatures. As a consequence, the effects of climate change might become evident earlier and be more devastating for hatchling production in the tropics. Loggerhead sea turtles (Caretta caretta) have the widest nesting range of any living reptile, spanning temperate to tropical latitudes in both hemispheres. Currently, loggerhead sea turtle populations in the tropics produce nearly 30% fewer hatchlings per nest than temperate populations. Strong correlations between empirical hatching success and habitat quality allowed global predictions of the spatiotemporal impacts of climate change on this fitness trait. Under climate change, many sea turtle populations nesting in tropical environments are predicted to experience severe reductions in hatchling production, whereas hatching success in many temperate populations could remain unchanged or even increase with rising temperatures. Some populations could show very complex responses to climate change, with higher relative hatchling production as temperatures begin to increase, followed by declines as critical physiological thresholds are exceeded more frequently. Predicting when, where, and how climate change could impact the reproductive output of local populations is crucial for anticipating how a warming world will influence population size, growth, and stability.

Variation in thermal performance of a widespread pathogen, the amphibian chytrid fungus Batrachochytrium dendrobatidis.

Rates of growth and reproduction of the pathogens that cause emerging infectious diseases can be affected by local environmental conditions; these conditions can thus influence the strength and nature of disease outbreaks. An understanding of these relationships is important for understanding disease ecology and developing mitigation strategies. Widespread emergence of the fungal disease chytridiomycosis has had devastating effects on amphibian populations. The causative pathogen, Batrachochytriumdendrobatidis (Bd), is sensitive to temperature, but its thermal tolerances are not well studied. We examined the thermal responses of three Bd isolates collected across a latitudinal gradient in eastern Australia. Temperature affected all aspects of Bd growth and reproduction that we measured, in ways that often differed among Bd isolates. Aspects of growth, reproduction, and their relationships to temperature that differed among isolates included upper thermal maxima for growth (26, 27, or 28 °C, depending on the isolate), relationships between zoospore production and temperature, and zoospore activity and temperature. Two isolates decreased zoospore production as temperature increased, whereas the third isolate was less fecund overall, but did not show a strong response to temperature until reaching the upper limit of its thermal tolerance. Our results show differentiation in life-history traits among isolates within Australia, suggesting that the pathogen may exhibit local adaptation. An understanding of how environmental temperatures can limit pathogens by constraining fitness will enhance our ability to assess pathogen dynamics in the field, model pathogen spread, and conduct realistic experiments on host susceptibility and disease transmission.

Forecasting range expansion into ecological traps: climate-mediated shifts in sea turtle nesting beaches and human development.

Some species are adapting to changing environments by expanding their geographic ranges. Understanding whether range shifts will be accompanied by increased exposure to other threats is crucial to predicting when and where new populations could successfully establish. If species overlap to a greater extent with human development under climate change, this could form ecological traps which are attractive to dispersing individuals, but the use of which substantially reduces fitness. Until recently, the core nesting range for the Critically Endangered Kemp's ridley sea turtle (Lepidochelys kempii) was ca. 1000 km of sparsely populated coastline in Tamaulipas, Mexico. Over the past twenty-five years, this species has expanded its range into populated areas of coastal Florida (>1500 km outside the historical range), where nesting now occurs annually. Suitable Kemp's ridley nesting habitat has persisted for at least 140 000 years in the western Gulf of Mexico, and climate change models predict further nesting range expansion into the eastern Gulf of Mexico and northern Atlantic Ocean. Range expansion is 6-12% more likely to occur along uninhabited stretches of coastline than are current nesting beaches, suggesting that novel nesting areas will not be associated with high levels of anthropogenic disturbance. Although the high breeding-site fidelity of some migratory species could limit adaptation to climate change, rapid population recovery following effective conservation measures may enhance opportunities for range expansion. Anticipating the interactive effects of past or contemporary conservation measures, climate change, and future human activities will help focus long-term conservation strategies.

Resilience of marine turtle regional management units to climate change.

Enhancing species resilience to changing environmental conditions is often suggested as a climate change adaptation strategy. To effectively achieve this, it is necessary first to understand the factors that determine species resilience, and their relative importance in shaping the ability of species to adjust to the complexities of environmental change. This is an extremely challenging task because it requires comprehensive information on species traits. We explored the resilience of 58 marine turtle regional management units (RMUs) to climate change, encompassing all seven species of marine turtles worldwide. We used expert opinion from the IUCN-SSC Marine Turtle Specialist Group (n = 33 respondents) to develop a Resilience Index, which considered qualitative characteristics of each RMU (relative population size, rookery vulnerability, and genetic diversity) and non climate-related threats (fisheries, take, coastal development, and pollution/pathogens). Our expert panel perceived rookery vulnerability (the likelihood of functional rookeries becoming extirpated) and non climate-related threats as having the greatest influence on resilience of RMUs to climate change. We identified the world's 13 least resilient marine turtle RMUs to climate change, which are distributed within all three major ocean basins and include six of the world's seven species of marine turtle. Our study provides the first look at inter- and intra-species variation in resilience to climate change and highlights the need to devise metrics that measure resilience directly. We suggest that this approach can be widely used to help prioritize future actions that increase species resilience to climate change.

Testing cost-benefit models of parental care evolution using lizard populations differing in the expression of maternal care.

Parents are expected to evolve tactics to care for eggs or offspring when providing such care increases fitness above the costs incurred by this behavior. Costs to the parent include the energetic demands of protecting offspring, delaying future fecundity, and increased risk of predation. We used cost-benefit models to test the ecological conditions favoring the evolution of parental care, using lizard populations that differ in whether or not they express maternal care. We found that predators play an important role in the evolution of maternal care because: (1) evolving maternal care is unlikely when care increases predation pressure on the parents; (2) maternal care cannot evolve under low levels of predation pressure on both parents and offspring; and (3) maternal care evolves only when parents are able to successfully defend offspring from predators without increasing predation risk to themselves. Our studies of one of the only known vertebrate species to exhibit interpopulation differences in the expression of maternal care provide clear support for some of the hypothesized circumstances under which maternal care should evolve (e.g., when nests are in exposed locations, parents are able to defend the eggs from predators, and egg incubation periods are brief), but do not support others (e.g., when nest-sites are scarce, life history strategies are "risky", reproductive frequency is low, and environmental conditions are harsh). We conclude that multiple pathways can lead to the evolution of parental care from a non-caring state, even in a single population of a widespread species.