Tuula A. Oksanen

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.

COST OF REPRODUCTION IN THE WILD: MANIPULATION OF REPRODUCTIVE EFFORT IN THE BANK VOLE

For three years, we manipulated litter size by adding or subtracting pups in eight wild populations of the bank vole, Clethrionomys glareolus, to examine reproductive costs and allocation of reproductive effort between offspring number and size. In general, litter enlargements did not increase the number of weanlings per mother and significantly decreased the size of weanlings. Reproductive effort and the breeding success of individuals varied within breeding seasons, but time of breeding and litter manipulation did not interact to affect reproductive trade-offs. Our 3-yr field experiment revealed that litter enlargements also reduced survival and fecundity of mothers. Small mammals have been considered typical income breeders, in which potential reproductive costs may be masked due to their ability to compensate for increased energetic demands of reproduction. Our results provide evidence that, in the wild, females may be incapable of escaping the costs of reproduction.

Testosterone‐Mediated Effects on Fitness‐Related Phenotypic Traits and Fitness

The physiological and behavioral mechanisms underlying life‐history trade‐offs are a continued source of debate. Testosterone (T) is one physiological factor proposed to mediate the trade‐off between reproduction and survival. We use phenotypic engineering and multiple laboratory and field fitness‐related phenotypic traits to test the effects of elevated T between two bank vole Myodes glareolus groups: dominant and subordinate males. Males with naturally high T levels showed higher social status (laboratory dominance) and mobility (distance between capture sites) than low‐T males, and the effect of T on immune response was also T group specific, suggesting that behavioral strategies may exist in male bank voles due to the correlated responses of T. Exogenous T enhanced social status, mate searching (polygon of capture sites), mobility, and reproductive success (relative measure of pups sired). However, exogenous T also resulted in the reduction of immune function, but only in males from the high‐T group. This result may be explained either by the immunosuppression costs of T or by differential sensitivity of different behavioral strategies to steroids. Circulating T levels were found to be heritable; therefore, female bank voles would derive indirect genetic benefits via good genes from mating with males signaling dominance.

Gonadotropin Hormone Modulation of Testosterone, Immune Function, Performance, and Behavioral Trade‐Offs among Male Morphs of the Lizard Uta stansburiana

Sexual selection predicts that trade‐offs maintain trait variation in alternative reproductive strategies. Experiments often focus on testosterone (T), but the gonadotropins follicle‐stimulating hormone and luteinizing hormone may provide a clearer understanding of the pleiotropic relationships among traits. We assess the activational role of gonadotropins on T and corticosterone regulation in traits expressed by polymorphic male side‐blotched lizards Uta stansburiana. Gonadotropins are found to enhance and suppress multiple physiological, morphological, and behavioral traits independently, as well as indirectly via T, and we demonstrate selective trade‐offs between reproduction and survival. The OBY locus, a genetic marker in our model vertebrate mating system, allows characterization of the interaction between genotype and hormone treatment on male traits. Our results suggest that oo, ob, and bb males are near their physiological and behavioral capacity for reproductive success, whereas yy and by males are maintained below their physiological maximum. Both by and yy morphs show trait plasticity, and we demonstrate that gonadotropins are likely proximate effectors that govern not only trait differences between alternative mating strategies but also morph plasticity. Gonadotropins clearly represent an important mechanism maintaining variation in physiological, morphological, and behavioral traits, as well as potentially maintaining the immunosuppression costs of male sexual signals.

Sex-specific selection on energy metabolism – selection coefficients for winter survival

Selection for different fitness optima between sexes is supposed to operate on several traits. As fitness‐related traits are often energetically costly, selection should also act directly on the energetics of individuals. However, efforts to examine the relationship between fitness and components of the energy budget are surprisingly scarce. We investigated the effects of basal metabolic rate (BMR, the minimum energy required for basic life functions) and body condition on long‐term survival (8 winter months) with manipulated densities in enclosed populations of bank voles (Myodes glareolus). Here, we show that survival selection on BMR was clearly sex‐specific but density‐independent. Both the linear selection gradient and selection differential for BMR were positive in females, whereas survival did not correlate with male characteristics. Our findings emphasize the relative importance of individual physiology over ecological factors (e.g. intra‐specific competition). Most current models of the origin of endothermy underline the importance of metabolic optima in females, whose physiology evolved to fulfil demands of parental provisioning in mammals. Our novel findings of sex‐specific selection could be related to these life history differences between sexes.

Offspring Defence in Relation to Litter Size and Age: Experiment in the Bank vole Clethrionomys glareolus

According to parental investment theory, nest defence activity should be related to the reproductive value of the offspring. Alternative hypotheses suggest that defence activity may, for example, depend upon the conspicuousness of the young. Studies concerning this topic have been carried out almost exclusively on birds and experimental data on the diversity of organisms is lacking. Bank voles Clethrionomys glareolus were used to study the effects of the number and age of offspring upon the pup defence activity of mothers. Male bank voles are infanticidal and thus an adult male was used as a predator. Defence trials were conducted in the laboratory and filmed for subsequent analysis. Litter sizes were divided into three treatment groups: reduced (−2 pups), control (±0 pups) and enlarged (+2 pups). In order to study the effect of offspring age upon maternal defence activity the trials were conducted twice: when the pups were 3 and 8 days old. Defence activity increased with the number of offspring and enlarged litters were most actively defended. This result supports parental investment theory and conclusions drawn by earlier studies of birds. However, in contrast to the conclusions of earlier studies, older offspring were defended less than the younger ones. Whilst new-born pups are totally defenceless against predators their vulnerability decreases as they age. Therefore, we suggest that maternal aggression in female bank voles is related to the value as well as to the vulnerability of the offspring. The validity of this explanation and the determinants of parental investment decisions in small mammals in general deserve further study.

Hormonal manipulation of offspring number: maternal effort and reproductive costs.

Abstract We used exogenous gonadotropin hormones to physiologically enlarge litter size in the bank vole (Clethrionomys glareolus). This method allowed the study design to include possible production costs of reproduction and a trade‐off between offspring number and body size at birth. Furthermore, progeny rearing and survival and postpartum survival of the females took place in outdoor enclosures to capture salient naturalistic effects that might be present during the fall and early winter. The aim of the study was to assess the effects of the manipulation on the growth and survival of the offspring and on the reproductive effort, survival, and future fecundity of the mothers. Mean offspring body size was smaller in enlarged litters compared to control litters at weaning, but the differences disappeared by the winter. Differences in litter sizes disappeared before weaning age due to higher mortality in enlarged litters. In addition to the effects of the litter size, offspring performance was probably also influenced by the ability of the mother to support the litter. Experimental females had higher reproductive effort at birth, and they also tended to have higher mortality during nursing. Combined effects of high reproductive effort at birth and high investment in nursing the litter entailed costs for the experimental females in terms of decreased probability of producing a second litter and a decreased body mass gain. Thus, enlarged litter size had both survival and fecundity costs for the mothers. Our results suggest that the evolution of litter size and reproductive effort is determined by reproductive costs for the mothers as well as by a trade‐off between offspring number and quality.

Intra‐ and Intersexual Trade‐Offs between Testosterone and Immune System: Implications for Sexual and Sexually Antagonistic Selection

Parasites indirectly affect life‐history evolution of most species. Combating parasites requires costly immune defenses that are assumed to trade off with other life‐history traits. In vertebrate males, immune defense is thought to trade off with reproductive success, as androgens enhancing sexual signaling can suppress immunity. The phenotypic relationship between male androgen levels and immune function has been addressed in many experimental studies. However, these do not provide information on either intra‐ or intersex genetic correlations, necessary for understanding sexual and sexually antagonistic selection theories. We measured male and female humoral antibody responses to a novel antigen (bovine gamma globulin), total immunoglobulin G, and the male testosterone level of a laboratory population of the bank vole (Myodes glareolus). Although we studied five traits, factor‐analytic modeling of the additive genetic (co)variance matrix within a restricted maximum likelihood–animal model supported genetic variation in three dimensions. Sixty‐five percent of the genetic variation contrasted testosterone with both immune measures in both sexes; consequently, selection for the male trait (testosterone) will have correlated effects on the immune system not only in males but also in females. Thus, our study revealed an intra‐ and intersexual genetic trade‐off between immunocompetence and male reproductive effort, of which only indirect evidence has existed so far.

Optimal allocation of reproductive effort: manipulation of offspring number and size in the bank vole

The number of offspring attaining reproductive age is an important measure of an individuals fitness. However, reproductive success is generally constrained by a trade–off between offspring number and quality. We conducted a factorial experiment in order to study the effects of an artificial enlargement of offspring number and size on the reproductive success of female bank voles (Clethrionomys glareolus). We also studied the effects of the manipulations on growth, survival and reproductive success of the offspring. Potentially confounding effects of varying maternal quality were avoided by cross–fostering. Our results showed that the number of offspring alive in the next breeding season was higher in offspring number manipulation groups, despite their smaller body size at weaning. Offspring size manipulation had no effect on offspring growth or survival. Further, the first litter size of female offspring did not differ between treatments. In conclusion, females may be able to increase the number of offspring reaching reproductive age by producing larger litters, whereas increasing offspring size benefits neither the mother nor the offspring.

Frequency and Density-Dependent Selection on Life-History Strategies – A Field Experiment

Negative frequency-dependence, which favors rare genotypes, promotes the maintenance of genetic variability and is of interest as a potential explanation for genetic differentiation. Density-dependent selection may also promote cyclic changes in frequencies of genotypes. Here we show evidence for both density-dependent and negative frequency-dependent selection on opposite life-history tactics (low or high reproductive effort, RE) in the bank vole (Myodes glareolus). Density-dependent selection was evident among the females with low RE, which were especially favored in low densities. Instead, both negative frequency-dependent and density-dependent selection were shown in females with high RE, which were most successful when they were rare in high densities. Furthermore, selection at the individual level affected the frequencies of tactics at the population level, so that the frequency of the rare high RE tactic increased significantly at high densities. We hypothesize that these two selection mechanisms (density- and negative frequency-dependent selection) may promote genetic variability in cyclic mammal populations. Nevertheless, it remains to be determined whether the origin of genetic variance in life-history traits is causally related to density variation (e.g. population cycles).