The evolution of life histories in garter snakes: Reproduction, aging, and the physiology of trade-offs

Life-history theory predicts that optimal life histories are shaped by trade-offs among traits expressed in different evolutionary and ecological contexts. Fast growth and high reproduction are predicted to trade off with lifespan, with the result that fast-living organisms will have shorter lives, while slow-living organisms will have longer lives. However, the generality of this theory for both determinately and indeterminately growing species, and the physiological mechanisms that underlie trade-offs, are poorly understood. We tested life-history theories of aging in natural populations of fast- and slow-living ecotypes of the indeterminately growing garter snake Thamnophis elegans. Long-term data on age-specific reproduction in both ecotypes revealed that neither showed signs of reproductive senescence even at the latest ages. Instead, both ecotypes continued to increase reproduction with age/size throughout life, with the fast-living ecotype increasing reproduction at a greater rate. These findings suggest that fast-living does not come at a cost to reproductive performance later in life. However, as the fast-living ecotype is known to exhibit shorter adult median lifespan than the slow-living ecotype in the field--a phenomenon proceeding from either extrinsic or intrinsic sources of mortality--we also tested for potential physiological mechanisms for trade-offs. Specifically, we tested for differences in immune defense between the two ecotypes, according to the ecoimmunological hypothesis that suggests fast-living populations should invest more in innate immunity than slow-living populations. As predicted, the fast-living ecotype showed higher levels of constitutive innate immunity than the slow-living ecotype. We also tested for differences in endocrine function between the two ecotypes. We predicted that the fast-living ecotype would exhibit higher levels of plasma insulin-like growth factor-1 (IGF-1), as high IGF-1 signaling is known to stimulate growth and reproduction at a cost to lifespan in model organisms. We found ecotype differences with respect to gravidity, body size, and annual climate, indicating that fast-living snakes may experience cumulatively higher levels of IGF-1 than slow-living snakes over their lifetimes. Thus IGF-1 may be an important mediator of life-history trade-offs in natural populations. Finally, through sequencing IGF-1 mRNA in a variety of reptile species, we found evidence that IGF-1 has been duplicated several times in the reptile lineage, which may have important for the physiology of life-history traits. All of these findings are discussed with reference to their contribution to the study of life-history evolution in general, with emphasis on the unique insights to be gained from the study of indeterminately growing species

Evolutionary ecology of endocrine-mediated life-history variation in the garter snake Thamnophis elegans

The endocrine system plays an integral role in the regulation of key life-history traits. Insulin-like growth factor-1 (IGF-1) is a hormone that promotes growth and reproduction, and it has been implicated in the reduction of lifespan. IGF-1 is also capable of responding plastically to environmental stimuli such as resource availability and temperature. Thus pleiotropic control of life-history traits by IGF-1 could provide a mechanism for the evolution of correlated life-history traits in a new or changing environment. An ideal system in which to investigate the role of IGF-1 in life-history evolution exists in two ecotypes of the garter snake Thamnophis elegans, which derive from a single recent ancestral source but have evolved genetically divergent life-history characteristics. Snakes from meadow populations near Eagle Lake, California (USA) exhibit slower growth rates, lower annual reproductive output, and longer median adult lifespans relative to populations along the lakeshore. We hypothesized that the IGF-1 system has differentiated between these ecotypes and can account for increased growth and reproduction and reduced survival in lakeshore vs. meadow snakes. We tested for a difference in plasma IGF-1 levels in free-ranging snakes from replicate populations of each ecotype over three years. IGF-1 levels were significantly associated with adult body size, reproductive output, and season in a manner that reflects established differences in prey ecology and age/size-specific reproduction between the ecotypes. These findings are discussed in the context of theoretical expectations for a trade-off between reproduction and lifespan that is mediated by pleiotropic endocrine mechanisms

Current and time‐lagged effects of climate on innate immunity in two sympatric snake species

Changing environments result in alterations at all levels of biological organization, from genetics to physiology to demography. The increasing frequency of droughts worldwide is associated with higher temperatures and reduced precipitation that can impact population persistence via effects on individual immune function and survival. We examined the effects of annual climate variation on immunity in two sympatric species of garter snakes from four populations in California over a seven‐year period that included the record‐breaking drought. We examined three indices of innate immunity: bactericidal competence (BC), natural antibodies (NABs), and complement‐mediated lysis (CL). Precipitation was the only climatic variable explaining variation in immune function: spring precipitation of the current year was positively correlated to Thamnophis sirtalis BC and NABs, whereas spring precipitation of the previous year was positively correlated to T. elegans BC and NABs. This suggests that T. elegans experiences a physiological time‐lag in response to reduced precipitation, which may reflect lack of capital for investment in immunity in the year following a dry year. In general, our findings demonstrate compelling evidence that climate can influence wild populations through effects on physiological processes, suggesting that physiological indices such as these may offer valuable opportunities for monitoring the effects of climate

The Utility of Reptile Blood Transcriptomes in Molecular Ecology

Reptiles and other non‐mammalian vertebrates have transcriptionally active nucleated red blood cells. If blood transcriptomes can provide quantitative data to address questions relevant to molecular ecology, this could circumvent the need to euthanize animals to assay tissues. This would allow longitudinal sampling of animals’ responses to treatments, as well as sampling of protected taxa. We developed and annotated blood transcriptomes from six reptile species. We found on average 25,000 proteins are being transcribed in the blood, and there is a CORE group of 9,282 orthogroups that are found in at least four of six species. In comparison to liver transcriptomes from the same taxa, approximately two‐thirds of the orthogroups were found in both blood and liver; and a similar percentage of ecologically relevant gene groups (insulin and insulin‐like signaling, electron transport chain, oxidative stress, glucocorticoid receptors) were found transcribed in both blood and liver. As a resource, we provide a user‐friendly database of gene ids identified in each blood transcriptome. Although, on average 37% of reads mapped to hemoglobin, importantly, the majority of non‐hemoglobin transcripts had sufficient depth (e.g., 97% at ≥10 reads) to be included in differential gene expression analysis. Thus, we demonstrate that RNAseq blood transcriptomes from a very small blood sample (\u3c10 μl) is a minimally invasive option in non‐mammalian vertebrates for quantifying expression of a large number of ecologically relevant genes that would allow longitudinal sampling and sampling of protected populations

The evolution of life histories in garter snakes: Reproduction, aging, and the physiology of trade-offs

Life-history theory predicts that optimal life histories are shaped by trade-offs among traits expressed in different evolutionary and ecological contexts. Fast growth and high reproduction are predicted to trade off with lifespan, with the result that "fast-living" organisms will have shorter lives, while "slow-living" organisms will have longer lives. However, the generality of this theory for both determinately and indeterminately growing species, and the physiological mechanisms that underlie trade-offs, are poorly understood. We tested life-history theories of aging in natural populations of fast- and slow-living ecotypes of the indeterminately growing garter snake Thamnophis elegans. Long-term data on age-specific reproduction in both ecotypes revealed that neither showed signs of reproductive senescence even at the latest ages. Instead, both ecotypes continued to increase reproduction with age/size throughout life, with the fast-living ecotype increasing reproduction at a greater rate. These findings suggest that fast-living does not come at a cost to reproductive performance later in life. However, as the fast-living ecotype is known to exhibit shorter adult median lifespan than the slow-living ecotype in the field--a phenomenon proceeding from either extrinsic or intrinsic sources of mortality--we also tested for potential physiological mechanisms for trade-offs. Specifically, we tested for differences in immune defense between the two ecotypes, according to the ecoimmunological hypothesis that suggests fast-living populations should invest more in innate immunity than slow-living populations. As predicted, the fast-living ecotype showed higher levels of constitutive innate immunity than the slow-living ecotype. We also tested for differences in endocrine function between the two ecotypes. We predicted that the fast-living ecotype would exhibit higher levels of plasma insulin-like growth factor-1 (IGF-1), as high IGF-1 signaling is known to stimulate growth and reproduction at a cost to lifespan in model organisms. We found ecotype differences with respect to gravidity, body size, and annual climate, indicating that fast-living snakes may experience cumulatively higher levels of IGF-1 than slow-living snakes over their lifetimes. Thus IGF-1 may be an important mediator of life-history trade-offs in natural populations. Finally, through sequencing IGF-1 mRNA in a variety of reptile species, we found evidence that IGF-1 has been duplicated several times in the reptile lineage, which may have important for the physiology of life-history traits. All of these findings are discussed with reference to their contribution to the study of life-history evolution in general, with emphasis on the unique insights to be gained from the study of indeterminately growing species.</p

Among-individual heterogeneity in maternal behaviour and physiology affects reproductive allocation and offspring life-history traits in the garter snake thamnophis elegans.

International audienceAccumulating evidence suggests that within‐individual plasticity of behavioural and physiological traits is limited, resulting in stable among‐individual differences in these aspects of the phenotype. Furthermore, these traits often covary within individuals, resulting in a continuum of correlated phenotypic variation among individuals within populations and species. This heterogeneity, in turn, affects individual fitness and can have cross‐generational effects. Patterns of trait covariation, among‐individual differences, and subsequent fitness consequences have long been recognized in reptiles. Here, we provide a test of patterns of among‐individual heterogeneity in behaviour and physiology and subsequent effects on reproduction and offspring fitness in the garter snake Thamnophis elegans. We find that measures of activity levels vary among individuals and are consistent within individuals in reproductive female snakes, indicating stable behavioural phenotypes. Blood hormone and glucose concentrations are not as stable within individuals, indicating that these traits do not describe consistent physiological phenotypes. Nonetheless, the major axes of variation in maternal traits describe behavioural and physiological phenotypes that interact to predict offspring body condition and mass at birth. This differential allocation of energy to offspring, in turn, strongly influences subsequent offspring growth and survival. This pattern suggests the potential for strong selection on phenotypes defined by behaviour–physiology interactions

Data from: Among-individual heterogeneity in maternal behaviour and physiology affects reproductive allocation and offspring life-history traits in the garter snake Thamnophis elegans

Accumulating evidence suggests that within-individual plasticity of behavioural and physiological traits is limited, resulting in stable among-individual differences in these aspects of the phenotype. Furthermore, these traits often covary within individuals, resulting in a continuum of correlated phenotypic variation among individuals within populations and species. This heterogeneity, in turn, affects individual fitness and can have cross-generational effects. Patterns of trait covariation, among-individual differences, and subsequent fitness consequences have long been recognized in reptiles. Here, we provide a test of patterns of among-individual heterogeneity in behaviour and physiology and subsequent effects on reproduction and offspring fitness in the garter snake Thamnophis elegans. We find that measures of activity levels vary among individuals and are consistent within individuals in reproductive female snakes, indicating stable behavioural phenotypes. Blood hormone and glucose concentrations are not as stable within individuals, indicating that these traits do not describe consistent physiological phenotypes. Nonetheless, the major axes of variation in maternal traits describe behavioural and physiological phenotypes that interact to predict offspring body condition and mass at birth. This differential allocation of energy to offspring, in turn, strongly influences subsequent offspring growth and survival. This pattern suggests the potential for strong selection on phenotypes defined by behaviour-physiology interactions

Social and demographic effects of anthropogenic mortality: a test of the compensatory mortality hypothesis in the red wolf.

Whether anthropogenic mortality is additive or compensatory to natural mortality in animal populations has long been a question of theoretical and practical importance. Theoretically, under density-dependent conditions populations compensate for anthropogenic mortality through decreases in natural mortality and/or increases in productivity, but recent studies of large carnivores suggest that anthropogenic mortality can be fully additive to natural mortality and thereby constrain annual survival and population growth rate. Nevertheless, mechanisms underlying either compensatory or additive effects continue to be poorly understood. Using long-term data on a reintroduced population of the red wolf, we tested for evidence of additive vs. compensatory effects of anthropogenic mortality on annual survival and population growth rates, and the preservation and reproductive success of breeding pairs. We found that anthropogenic mortality had a strong additive effect on annual survival and population growth rate at low population density, though there was evidence for compensation in population growth at high density. When involving the death of a breeder, anthropogenic mortality was also additive to natural rates of breeding pair dissolution, resulting in a net decrease in the annual preservation of existing breeding pairs. However, though the disbanding of a pack following death of a breeder resulted in fewer recruits per litter relative to stable packs, there was no relationship between natural rates of pair dissolution and population growth rate at either high or low density. Thus we propose that short-term additive effects of anthropogenic mortality on population growth in the red wolf population at low density were primarily a result of direct mortality of adults rather than indirect socially-mediated effects resulting in reduced recruitment. Finally, we also demonstrate that per capita recruitment and the proportion of adults that became reproductive declined steeply with increasing population density, suggesting that there is potential for density-dependent compensation of anthropogenically-mediated population regulation

Corticosterone and pace of life in two life-history ecotypes of the garter snake thamnophis elegans

Glucocorticoids are main candidates for mediating life-history trade-offs by regulating the balance between current reproduction and survival. It has been proposed that slow-living organisms should show higher stress-induced glucocorticoid levels that favor self-maintenance rather than current reproduction when compared to fast-living organisms. We tested this hypothesis in replicate populations of two ecotypes of the garter snake (Thamnophis elegans) that exhibit slow and fast pace of life strategies. We subjected free-ranging snakes to a capture-restraint protocol and compared the stress-induced corticosterone levels between slow- and fast-living snakes. We also used a five-year dataset to assess whether baseline corticosterone levels followed the same pattern as stress-induced levels in relation to pace of life. In accordance with the hypothesis, slow-living snakes showed higher stress-induced corticosterone levels than fast-living snakes. Baseline corticosterone levels showed a similar pattern with ecotype, although differences depended on the year of study. Overall, however, levels of glucocorticoids are higher in slow-living than fast-living snakes, which should favor self-maintenance and survival at the expense of current reproduction. The results of the present study are the first to relate glucocorticoid levels and pace of life in a reptilian system and contribute to our understanding of the physiological mechanisms involved in life-history evolution.Fil: Palacios, María Gabriela. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Centro Nacional Patagónico; Argentina. University of Iowa; Estados UnidosFil: Sparkman, Amanda M.. University of Iowa; Estados UnidosFil: Bronikowski, Anne M.. University of Iowa; Estados Unido

Current and time‐lagged effects of climate on innate immunity in two sympatric snake species

Changing environments result in alterations at all levels of biological organization, from genetics to physiology to demography. The increasing frequency of droughts worldwide is associated with higher temperatures and reduced precipitation that can impact population persistence via effects on individual immune function and survival. We examined the effects of annual climate variation on immunity in two sympatric species of garter snakes from four populations in California over a seven‐year period that included the record‐breaking drought. We examined three indices of innate immunity: bactericidal competence (BC), natural antibodies (NABs), and complement‐mediated lysis (CL). Precipitation was the only climatic variable explaining variation in immune function: spring precipitation of the current year was positively correlated to Thamnophis sirtalis BC and NABs, whereas spring precipitation of the previous year was positively correlated to T. elegans BC and NABs. This suggests that T. elegans experiences a physiological time‐lag in response to reduced precipitation, which may reflect lack of capital for investment in immunity in the year following a dry year. In general, our findings demonstrate compelling evidence that climate can influence wild populations through effects on physiological processes, suggesting that physiological indices such as these may offer valuable opportunities for monitoring the effects of climate. This article is published as Combrink, Lucia L., Anne M. Bronikowski, David AW Miller, and Amanda M. Sparkman. "Current and time‐lagged effects of climate on innate immunity in two sympatric snake species." Ecology and Evolution (2021). doi: 10.1002/ece3.7273.</p