Barry Sinervo

Erosion of lizard diversity by climate change and altered thermal niches

Demise of the Lizards Despite pessimistic forecasts from recent studies examining the effects of global climate change on species, and observed extinctions in local geographic areas, there is little evidence so far of global-scale extinctions. Sinervo et al. (p. 894; see the Perspective by Huey et al.) find that extinctions resulting from climate change are currently reducing global lizard diversity. Climate records during the past century were synthesized with detailed surveys of Mexican species at 200 sites over the past 30 years. Temperature change has been so rapid in this region that rates of adaptation have not kept pace with climate change. The models were then extended to all families of lizards at >1000 sites across the globe, and suggest that climate change-induced extinctions are currently affecting worldwide lizard assemblages. A historical record of lizard populations in Mexico is used to parameterize models that predict global effects of climate change. It is predicted that climate change will cause species extinctions and distributional shifts in coming decades, but data to validate these predictions are relatively scarce. Here, we compare recent and historical surveys for 48 Mexican lizard species at 200 sites. Since 1975, 12% of local populations have gone extinct. We verified physiological models of extinction risk with observed local extinctions and extended projections worldwide. Since 1975, we estimate that 4% of local populations have gone extinct worldwide, but by 2080 local extinctions are projected to reach 39% worldwide, and species extinctions may reach 20%. Global extinction projections were validated with local extinctions observed from 1975 to 2009 for regional biotas on four other continents, suggesting that lizards have already crossed a threshold for extinctions caused by climate change.

Genome 10K: A Proposal to Obtain Whole-Genome Sequence for 10 000 Vertebrate Species

The human genome project has been recently complemented by whole-genome assessment sequence of 32 mammals and 24 nonmammalian vertebrate species suitable for comparative genomic analyses. Here we anticipate a precipitous drop in costs and increase in sequencing efficiency, with concomitant development of improved annotation technology and, therefore, propose to create a collection of tissue and DNA specimens for 10,000 vertebrate species specifically designated for whole-genome sequencing in the very near future. For this purpose, we, the Genome 10K Community of Scientists (G10KCOS), will assemble and allocate a biospecimen collection of some 16,203 representative vertebrate species spanning evolutionary diversity across living mammals, birds, nonavian reptiles, amphibians, and fishes (ca. 60,000 living species). In this proposal, we present precise counts for these 16,203 individual species with specimens presently tagged and stipulated for DNA sequencing by the G10KCOS. DNA sequencing has ushered in a new era of investigation in the biological sciences, allowing us to embark for the first time on a truly comprehensive study of vertebrate evolution, the results of which will touch nearly every aspect of vertebrate biological enquiry.

Behavioral Drive versus Behavioral Inertia in Evolution: A Null Model Approach

Some biologists embrace the classical view that changes in behavior inevitably initiate or drive evolutionary changes in other traits, yet others note that behavior sometimes inhibits evolutionary changes. Here we develop a null model that quantifies the impact of regulatory behaviors (specifically, thermoregulatory behaviors) on body temperature and on performance of ectotherms. We apply the model to data on a lizard (Anolis cristatellus) and show that thermoregulatory behaviors likely inhibit selection for evolutionary shifts in thermal physiology with altitude. Because behavioral adjustments are commonly used by ectotherms to regulate physiological performance, regulatory behaviors should generally constrain rather than drive evolution, a phenomenon we call the “Bogert effect.” We briefly review a few other examples that contradict the classical view of behavior as the inevitable driving force in evolution. Overall, our analysis and brief review challenge the classical view that behavior is invariably the driving force in evolution, and instead our work supports the alternative view that behavior has diverse—and sometimes conflicting—effects on the directions and rates at which other traits evolve.

The evolution of maternal investment in lizards : an experimental and comparative analysis of egg size and its effects on offspring performance

I used comparative and experimental analysis of egg size in a Sceloporus lizard to examine a fundamental tenet of life‐history theory: the presumed trade‐offs among offspring number, offspring size, and performance traits related to offspring size that are likely to influence fitness. I analyzed latitudinal and elevational patterns of egg life‐history characteristics among populations and experimentally manipulated egg size and hatchling size by removing yolk from the eggs to examine the causal bases of population differences in offspring traits.

Density cycles and an offspring quantity and quality game driven by natural selection.

A long-standing hypothesis posits that natural selection can favour two female strategies when density cycles. At low density, females producing many smaller progeny are favoured when the intrinsic rate of increase, r, governs population growth. At peak density, females producing fewer, high-quality, progeny are favoured when the carrying capacity, K, is exceeded and the population crashes. Here we report on the first example of a genetic r versus K selection game that promotes stable population cycles in lizards. Decade-long fitness studies and game theory demonstrated that two throat-colour morphs were refined by selection in which the strength of natural selection varied with density. Orange-throated females, r strategists, produced many eggs and were favoured at low density. Conversely, yellow-throated females, K strategists, produced large eggs and were favoured at high density. Progeny size should also be under negative frequency-dependent selection in that large progeny will have a survival advantage when rare, but the advantage disappears when they become common. We confirmed this prediction by seeding field plots with rare and common giant hatchlings. Thus, intrinsic causes of frequency- and density-dependent selection promotes an evolutionary game with two-generation oscillations.

Correlational selection and the evolution of genomic architecture

We review and discuss the importance of correlational selection (selection for optimal character combinations) in natural populations. If two or more traits subject to multivariate selection are heritable, correlational selection builds favourable genetic correlations through the formation of linkage disequilibrium at underlying loci governing the traits. However, linkage disequilibria built up by correlational selection are expected to decay rapidly (ie, within a few generations), unless correlational selection is strong and chronic. We argue that frequency-dependent biotic interactions that have ‘Red Queen dynamics’ (eg, host-parasite interactions, predator-prey relationships or intraspecific arms races) often fuel chronic correlational selection, which is strong enough to maintain adaptive genetic correlations of the kind we describe. We illustrate these processes and phenomena using empirical examples from various plant and animal systems, including our own recent work on the evolutionary dynamics of a heritable throat colour polymorphism in the side-blotched lizard Uta stansburiana. In particular, male and female colour morphs of side-blotched lizards cycle on five- and two-generation (year) timescales under the force of strong frequency-dependent selection. Each morph refines the other morph in a Red Queen dynamic. Strong correlational selection gradients among life history, immunological and morphological traits shape the genetic correlations of the side-blotched lizard polymorphism. We discuss the broader evolutionary consequences of the buildup of co-adapted trait complexes within species, such as the implications for speciation processes.

Testosterone, Endurance, and Darwinian Fitness: Natural and Sexual Selection on the Physiological Bases of Alternative Male Behaviors in Side- Blotched Lizards

The mechanistic bases of natural and sexual selection on physiological and behavioral traits were examined in male morphs of three colors of the side-blotched lizard, Uta stansburiana. Orange-throated males are aggressive and defend large territories with many females. Blue-throated males defend smaller territories with fewer females; however, blue-throated males assiduously mate guard females on their territory. Yellow-throated males do not defend a territory, but patrol a large home range. They obtain secretive copulations from females on the territories of dominant males. Males with bright orange throats had higher levels of plasma testosterone (T), endurance, activity, and home range size and concomitantly gained greater control over female home ranges than blue- or yellow-throated males. Experimentally elevating plasma T in yellow- and blue-throated males increased their endurance, activity, home range size, and control over female territories to levels that were seen in unmanipulated orange-throated males that had naturally high plasma T. However, the enhanced performance of orange-throated males is not without costs. Orange-throated males had low survival compared to the other morphs. Finally, some yellow-throated males transformed to a partial blue morphology late in the season and the endurance of these transforming yellow-throated males increased from early to late in the season. In addition, yellow-throated males that transformed to blue also had significantly higher plasma T late in the season compared to the plasma T earlier in the season. T appears to play an important role in the physiological changes that all three color morphs undergo during the process of maturation. In some yellow males, T plays an additional role in plastic changes in behavior and physiology late in the reproductive season. We discuss natural and sexual selection on physiological and behavioral traits that leads to the evolution of steroid regulation in the context of alternative male strategies.

Proximate Constraints on the Evolution of Egg Size, Number, and Total Clutch Mass in Lizards

Proximate constraints on egg size, number, and total clutch mass in side-blotched lizards were examined by experimentally reducing average clutch size from 4.6 eggs to one, two, and three eggs. Eggs from experimentally altered clutches were larger than those from controls, reflecting the trade-off between egg size and number. Moreover, the increased frequency of females with oviducally bound eggs or eggs that burst at oviposition suggests that egg size in clutches with very few eggs are at a functional upper size limit. These proximate constraints may also limit evolution of egg size in another group of lizards (Anolis) that only produces one-egged clutches.

Costs of reproduction in the wild: Path analysis of natural selection and experimental tests of causation

During 1991 through 1994, natural selection on reproductive effort in side‐blotched lizards was indexed by measuring total clutch mass produced on the first clutch of the reproductive season and assessing how such effort in current reproduction affects subsequent survival and clutch production. In addition, selection was also experimentally assessed in free‐ranging female side‐blotched lizards by (1) surgically decreasing total clutch mass (direct ovarian manipulation) and enhancing clutch mass using (2) exogenous gonadotropin, and (3) exogenous corticosterone. Surgical reduction of clutch mass uniformly enhanced survival. However, increasing clutch mass had more complex effects depending on year. Experimentally enhanced clutch mass enhanced survival in 1991, had no effect on survival in 1992, and decreased survival in 1993. Despite the complexity of these experimental results, they are corroborated by our comparative data. It is important to note that local environmental effects can obscure detection of costs arising from natural variation in reproductive effort, and we removed such effects using path analysis. The striking shift in natural selection favoring females laying a large clutch mass (1991) to selection against females laying a large clutch mass (1993) is associated with an end of a severe multiyear drought. Our natural‐history observations suggest that the correlated increase in predatory snake activity on our study site, coincident with the end of the drought, is the agent of natural selection. Although the actual agents of selection (e.g., snake predation versus drought‐related effects) are not resolved, the patterns of natural selection measured in our comparative and experimental data are also consistent with year‐to‐year changes in clutch mass and egg size that would be indicative of rapid short‐term evolution in these traits.

Allometric Engineering: An Experimental Test of the Causes of Interpopulational Differences in Performance

Hatchling lizards (Sceloporus occidentalis) from a southern population are large and have high locomotor performance (speed and stamina) relative to hatchlings from northern populations. In order to determine whether differences in performance are an allometric consequence of interpopulation differences in size, yolk was removed from southern eggs, thereby producing miniaturized hatchlings equivalent in size to northern hatchlings. Miniaturized southern hatchlings no longer had higher speed than northern hatchlings, but maintained higher stamina. Interpopulation differences in speed but not in stamina are thus an allometric consequence of differences in egg size. Size manipulation adds an experimental dimension to aliometric analyses.