The UCSC University Library Synergy Lecture Series is excited to welcome Distinguished Professor Dr. Barry Sinervo as our Synergy Lecturer for Spring 2013.  He will present a climate change extinction model that has been validated by known lizard extinctions, and explain how this model can be extended to other vertebrates.

Presented April 24, 2013, 3-4pm in the  Ching-Yi Dougherty Reading Room of the UCSC Science & Engineering Library.

The evolutionary diversification of many terrestrial vertebrate groups is strongly linked to climatic events in the Cenozoic, the period from 65 Million years ago to today when modern animals first appeared. I investigated the effects of Cenozoic climate change on the taxonomic and morphological diversification of the Old World lizard family Lacertidae, with particular emphasis on the African radiation. African lacertids exhibit an unusual pattern of diversification, in which their highest species richness occurs in deserts north and south of the equator, despite being spread throughout the continent. This disparity is particularly surprising given that desert lacertids are thought to be evolutionarily younger than their mesic-dwelling relatives, suggesting increased diversification rates in arid habitats. To identify the evolutionary factors underlying this pattern, I use a combination of phylogenetic, morphological and ecological techniques. In Chapter 1, I apply Bayesian methods and fossil-based calibrations to molecular sequence data to construct a time-calibrated phylogeny for Lacertidae. I estimate that the family arose in the early Cenozoic, with the majority of their African radiation occurring in the Eocene and Oligocene. In Chapter 2, I describe changes in lacertid body shape across biomes and substrates, and find widespread morphological convergence in similar habitat types. I suggest that in addition to foraging demands, fluctuating and extreme climatic conditions, largely driven by precipitation and temperature, contribute to morphological convergence across independent arid-dwelling clades. Finally, I test if ancestral transitions in ecology, morphology, and rates of diversification temporally coincide with paleoclimatic events in the Cenozoic. I use High Resolution X-ray Computed Tomography to characterize changes in the skull related to life in arid habitats, and apply maximum likelihood methods to test if the origins of those traits temporally coincide with significant shifts in habitat, diversification rates and climatic changes. My results show that African lacertids experienced three major peaks in diversification, accompanied by the evolution of suites of arid-adapted morphological traits. These changes coincide with climatic shifts in Africa, including the transition from closed forests to open grasslands and savanna in the late Oligocene, prior to the peak temperatures of the mid-Miocene Climatic Optimum, and following the formation of the Benguela current leading to hyper-aridity in southern Africa. I conclude that deserts are important centers for reptile evolution, but that expected changes in climate due to global warming may outpace the ability of arid-dwelling species to adapt and persist in the future.

Female preference for higher quality males can influence both intrasexual and intersexual dynamics. In species with biparental care, male quality can influence not only the female's initial gametic investment but also the amount of care each parent provides to the offspring. Here, I describe studies of female reproductive investment in response to male size, an indicator of quality, and the effect of female intrasexual selection on parental behavior in the convict cichlid (Amatitlania siquia), a monogamous, biparental fish.

In Chapter 1, I observed breeding patterns in a natural population in Costa Rica and found that females increased their parental care when paired with larger males. Male size was positively correlated with offspring number, indicating a benefit to females from pairing with larger males. In Chapter 2, using a controlled breeding experiment, I investigated trade-offs in female fecundity and parental care within and between breeding events in response to male size. I found that females initially paired with small males had a greater probability of failing to successfully breed. Females did not increase their fecundity when paired with large males, but did increase their parental care and defensive behaviors. However, females did not benefit from pairing with larger males because they had fewer offspring. Male size did not significantly affect female parental care behavior during the second breeding, and fecundity again did not differ between females paired with small and large males. In Chapter 3, I presented breeding pairs with non-reproductive and reproductive female conspecific intruders. I found that parental females behaved more aggressively towards reproductive intruders, which were a threat to their mating status, compared to non-reproductive intruders, which were only a threat to their offspring. Female size, rather than male size, predicted parental female response to intruders, with small females behaving more aggressively. Males preferred to associate with the reproductive intruder, as it represented a potential new mate.

The results of this dissertation demonstrate that females increase their parental care, but not their fecundity, for larger males. Moreover, females appear to use their prior breeding experience when allocating resources to the current reproductive event, as females did not increase their parental care when paired with large males during their second mating because large males failed to provide any benefits during the initial breeding. Male quality influences intersexual dynamics, but not intrasexual interactions, suggesting that females may be altering their response to the threat of male desertion. Overall, these results suggest that increased female investment may stabilize the pair-bond between the parents, which ultimately increases female reproductive success.

The merging of empirical tests and theoretical models allows us to make sense of complex biological concepts. This thesis explores questions of biological variation (both within and between species) and its persistence through evolutionary time scales primarily through the development of mechanistic models. The first chapter uses a game theory framework to describe drivers of persistence in systems of alternative strategies, and presents a new framework to describe competition within large systems. The second chapter describes the plastic system of developmental polyphenisms in the Mexican spadefoot toads, Scaphiopus multiplicata using a game theory framework. The possibility that anthropogenic climate change will alter selection on developmental polyphenisms is explored. The third chapter uses a mechanistic ecophysiology-based model to explore extinction risk in seven species of tropical New World day geckos (Sphaerodactylidae, Squamata). These studies highlight the importance of incorporating empirical data in modeling. Given anthropogenic changes to climate and habitat availability, ecosystem resilience of particular concern to conservationists. We need tools to predict how species losses will affect eventual equilibrium outcomes – whether ecosystems will survive in a recognizable state, or whether the loss of key species can affect larger-scale stability.

Life on earth is in the midst of an extinction crisis. Modern rates of extinction are comparable to rates of extinction during the five mass extinction events of the Phanerozoic. While habitat loss and invasive species have been dominant historical drivers of extinction, climate change is projected to emerge as a codominant driver of extinction during the 21st century. This dissertation explores the impacts of climate change, habitat loss, and invasive species on California wildlife with the goal of providing information that will assist in conserving biodiversity. Two themes that unite this dissertation are conservation biogeography and climate change. The first two chapters focus on historical and projected climate-mediated range contraction in a species that appears to be threatened almost entirely by climate change, as opposed to other sources of decline. Chapter three assesses the vulnerability of twenty California mammal species to climate change and includes consideration of land use, hydroclimatic niche, dispersal ability, sea level rise, and species traits. Chapter four explores strategies for recovering one of the first species to be protected under endangered species law in the context of habitat loss, invasive species, climate change, habitat protection, and potential for habitat restoration on retired farmland.

Discrete variation in colorful sexual signals is often associated with variation in reproductive tactics or strategies. Many taxa with intrapopulation color polymorphisms also exhibit variation among populations or among closely related species in the frequency of color morphs, the number of morphs present within a population, or which particular colors are used as signals. These patterns may be important for understanding speciation because theoretical and empirical studies indicate that both color polymorphism and alternative reproductive tactics may be associated with elevated diversification rates. I studied variation in throat color, an important sexual signal, within and among populations of the mesquite lizard (Sceloporus grammicus) species complex. The S. grammicus species complex is considered a possible example of incipient speciation due to high levels of variation in chromosome number, habitat use, reproductive cycles, and life history. My first chapter confirms this variability in female life history, and the rest of my dissertation is the first research to address sexual signals in S. grammicus. I performed a broad geographic survey of throat color polymorphisms and used laboratory behavioral trials and molecular phylogenetics to investigate the meaning and evolutionary context of the polymorphisms I observed. I found that male S. grammicus within a single population exhibited either orange, yellow, and blue throat color morphs or orange, yellow, and white throat color morphs. In no case did I observe the blue male morph and the white male morph in the same population. I found that both the orange/yellow/blue and orange/yellow/white polymorphisms in males were associated with variation in male aggression level, but the meanings of particular colors were different between the two populations I studied.

I also found that females performed more rejection behaviors towards allopatric males when those males were of a color morph that did not occur in the female's home population than when the allopatric male was of a color morph that did occur in the female's home population. Finally, I constructed a phylogeny of the populations I had sampled and used ancestral state reconstruction to establish that the white male morph in the S. grammicus complex has originated at least twice.

Climate change is predicted to severely impact species distributions and extinction risk in the coming decades. Ectotherms, such as lizards, are of particular concern due to their dependence on environmental temperatures to survive and reproduce. The predictions of extreme weather events and increases in global mean temperatures will affect the ability of these organisms to carry out important functions such as feeding or breeding. While we predict that these organisms will face challenges from climate change, examining whether they show evidence of coping with these changes is critical for determining extinction risk and making conservation decisions. In this dissertation, I use treatments of 3-hour (short), 6-hour (mid/control), and 9-hour (long) access to basking heat to investigate how different climate extremes, predicted to increase and worsen under climate change, would impact various aspects of pregnant viviparous European common lizards (Zootoca vivipara). The 3-hour treatments reflect an unusually long series of cool days limiting thermoregulation, 6-hours reflects the “normal” period of contemporary climate and 9-hours reflects periods of long-duration heat spells.

In Chapter 1, I look at the flexibility of females to modify their behavior to different basking treatments and how intraspecific variation between populations plays a role. My results demonstrate these lizards exhibit plasticity in basking behavior in response to varying thermal opportunity. However, the magnitude to which they modify their behavior is significantly tempered by environmental characteristics of their population of origin. In Chapter 2, I investigate how basking treatments influence gestation and offspring phenotype, as the offspring life history stage is one of great importance. We found that offspring phenotype was significantly affected by mother basking treatments with local population differences and sex-dependent outcomes on size and viability in juveniles. My findings indicate that cooler and warmer temperatures have different effects on progeny phenotype and may have cascading impacts under climate change in the next generation. In Chapter 3, I examine how parasite load varies between populations and whether basking treatments influence a lizard’s ability to fight infection. The basking treatments influenced changes in parasite load in three of the five populations, where we observed a relatively small increase in parasite abundance in lizards in the short and mid/control basking treatment compared to the long treatment. This difference between populations suggests a context-dependent impact of basking opportunities on the capability of lizards to clear parasite infections, under the warm environment treatment (9-h) and provides further evidence that ectothermic host-blood parasite relationships are likely to be impacted by future and contemporary climate change.

The results of this dissertation ultimately highlight the complex impacts climate change can have on these organisms and will hopefully encourage further research while raising awareness of this pressing issue.

Biological processes underlying species responses to climate, such as physiology, phenology and demography, can add important information to the prediction of climate change effects on organisms, yet most studies do not consider those processes. On this thesis, I present and evaluate different venues of incorporating such processes on biogeographical analysis. On the first chapter, I show activity time can be a better predictor than environmental temperatures for the distribution a tropical lizard, Tropidurus torquatus. I also determine the best practices for obtaining those estimates. Tropidurus torquatus seems to be restricted in its distributions by colder temperatures and precipitation, thus climate warming could lead to potential range expansion. On the second chapter, I examine the drivers of reproductive seasonality in two tropical lizards, Tropidurus torquatus and Ameiva ameiva. Solar radiation and day length were the main factors determining the reproductive seasonality of T. torquatus, while A. ameiva was more sensitive to precipitation. Solar radiation could be driving T. torquatus breeding phenology through the parietal eye mechanism, while A. ameiva, which lacks such structure, could be more sensitive to immediate weather conditions. This might have important consequences for these T. torquatus adaptation to climate change, since the rapid shift in weather might cause a mismatch between the photoperiodic cue and optimal environmental conditions for reproduction. On the third chapter, I use the estimates of time of activity and breeding phenology o from the previous chapters to spatially extrapolate demographic rates obtained from a 12-year mark and recapture study on a T. torquatus population. Survival was correlated with time of activity and precipitation, both interacting with breeding phenology, while recruitment was correlated with temperature and precipitation, with no breeding season interaction. Population growth projections were not correlated with occurrence records, indicating that spatial predictions were unreliable. Physiology and phenology add important information to the estimation of demographic rates at local scales but proved unreliable predictors for spatial extrapolation of those rates. This could be due to environmental variation, adaptation, plasticity or species interactions. We suggest possible venues for incorporating those processes and improving similar analysis. I provide an R package, Mapinguari, with tools to generate spatial predictors based on the processes described here.