Destabilized host-parasite dynamics in newly founded populations.

When species disperse into previously unoccupied habitats, new populations encounter unfamiliar species interactions such as altered parasite loads. Theory predicts that newly founded populations should exhibit destabilized eco-evolutionary fluctuations in infection rates and immune traits. However, to understand founder effects biologists typically rely on retrospective studies of range expansions, missing early-generation infection dynamics. To remedy this, we experimentally founded whole-lake populations of threespine stickleback. Infection rates were temporally stable in native source lakes. In contrast, newly founded populations exhibit destabilized host-parasite dynamics: high starting infection rates led to increases in a heritable immune trait (peritoneal fibrosis), suppressing infection rates. The resulting temporal auto-correlation between infection and immunity suggest that newly founded populations can exhibit rapid host-parasite eco-evolutionary dynamics.

Broad Concordance in the Spatial Distribution of Adaptive and Neutral Genetic Variation across an Elevational Gradient in Deer Mice.

When species are continuously distributed across environmental gradients, the relative strength of selection and gene flow shape spatial patterns of genetic variation, potentially leading to variable levels of differentiation across loci. Determining whether adaptive genetic variation tends to be structured differently than neutral variation along environmental gradients is an open and important question in evolutionary genetics. We performed exome-wide population genomic analysis on deer mice sampled along an elevational gradient of nearly 4,000 m of vertical relief. Using a combination of selection scans, genotype-environment associations, and geographic cline analyses, we found that a large proportion of the exome has experienced a history of altitude-related selection. Elevational clines for nearly 30% of these putatively adaptive loci were shifted significantly up- or downslope of clines for loci that did not bear similar signatures of selection. Many of these selection targets can be plausibly linked to known phenotypic differences between highland and lowland deer mice, although the vast majority of these candidates have not been reported in other studies of highland taxa. Together, these results suggest new hypotheses about the genetic basis of physiological adaptation to high altitude, and the spatial distribution of adaptive genetic variation along environmental gradients.

Metabolic Rates Predict Baseline Corticosterone and Reproductive Output in a Free-Living Passerine.

Organisms continuously face environmental fluctuations, and allocation of metabolic investment to meet changing energetic demands is fundamental to survival and reproductive success. Glucocorticoid (GC) hormones (e.g., corticosterone [CORT]) play an important role in energy acquisition and allocation in the face of environmental challenges, partly through mediation of energy metabolism. Although GCs and metabolic rate are expected to covary, surprisingly few empirical studies have demonstrated such relationships, especially in wild animals. Moreover, studies testing for associations between GCs and fitness generally do not account for among-individual differences in energy expenditure or energy allocation. We measured CORT (baseline and stress-induced) and metabolic traits (resting metabolic rate [RMR], cold-induced VO2max [Msum], and aerobic scope [the difference between Msum and RMR]) in female tree swallows (Tachycineta bicolor) during chick-rearing, and tested for their associations with several variables of reproductive performance. We found a positive relationship between RMR and baseline CORT, but no consistent associations between stress-induced CORT (SI-CORT) and Msum. This suggests that while baseline CORT may be a good indicator of an individual's baseline metabolic investment, SI-CORT responses are not associated with aerobic scope or the upper limits of aerobic performance. Furthermore, we found that metabolic traits were associated with reproductive performance: females with higher reproductive output showed higher Msum, and also tended to show higher RMR. Overall, these results suggest that metabolic traits are better predictors of reproductive output in tree swallows than CORT concentrations. They further point to the maximal aerobic capacity being higher in females investing more heavily in a current reproductive event, but whether this association reflects trade-offs between current and future reproductive efforts remains to be tested.

Los organismos se enfrentan continuamente a fluctuaciones ambientales, y la distribución de la inversión metabólica es fundamental para la supervivencia y el éxito reproductivo ante demandas energéticas cambiantes. Las hormonas glucocorticoides (GC), como la corticosterona (CORT), juegan un papel importante en los procesos de adquisición y distribución de energía durante los desafíos ambientales, en parte a través de su papel mediador del metabolismo energético. Aunque es esperable que los GCs y la tasa metabólica covaríen, muy pocos estudios empíricos han demostrado esta relación, especialmente en animales salvajes. Además, los estudios que han testado la asociación entre GCs y eficacia biológica normalmente no tienen en cuenta las diferencias en gasto o distribución energética existentes entre individuos. En este estudio, medimos CORT (basal e inducida por estrés) y parámetros metabólicos [tasa metabólica en reposo (RMR), VO2max inducido por frío (Msum) y el alcance metabólico (la diferencia entre Msum y RMR)] en hembras de golondrina bicolor (Tachycineta bicolor) durante el período de crianza de los pollos, y testamos sus asociaciones con varios parámetros reproductivos. Encontramos una relación positiva entre RMR y CORT basal, pero ninguna asociación consistente entre CORT inducida por el estrés y Msum. Esto sugiere que mientras que la CORT basal sería un buen indicador individual del gasto metabólico base, las respuestas de CORT inducidas por estrés no están asociadas con el alcance metabólico o con los límites superiores del rendimiento aeróbico. Encontramos, además, una asociación entre parámetros metabólicos y reproducción: las hembras con mayor éxito reproductivo mostraron mayor Msum, y una tendencia a mostrar mayor RMR. A nivel general, estos resultados sugieren que los parámetros metabólicos son mejores predictores del éxito reproductivo que los niveles de CORT en la golondrina bicolor. También apuntan a que la capacidad aeróbica máxima es mayor en aquellas hembras que invierten más intensamente en el evento reproductivo actual, pero queda por investigar si esta asociación refleja compromisos entre esfuerzo reproductivo actual y futuro.

Ecology, not distance, explains community composition in parasites of sky-island Audubon's Warblers.

Haemosporidian parasites of birds are ubiquitous in terrestrial ecosystems, but their coevolutionary dynamics remain poorly understood. If species turnover in parasites occurs at a finer scale than turnover in hosts, widespread hosts would encounter diverse parasites, potentially diversifying as a result. Previous studies have shown that some wide-ranging hosts encounter varied haemosporidian communities throughout their range, and vice-versa. More surveys are needed to elucidate mechanisms that underpin spatial patterns of diversity in this complex multi-host multi-parasite system. We sought to understand how and why a community of avian haemosporidian parasites varies in abundance and composition across elevational transects in eight sky islands in southwestern North America. We tested whether bird community composition, environment, or geographic distance explain haemosporidian parasite species turnover in a widespread host that harbors a diverse haemosporidian community, the Audubon's Warbler (Setophaga auduboni). We tested predictors of infection using generalized linear models, and predictors of bird and parasite community dissimilarity using generalized dissimilarity modeling. Predictors of infection differed by parasite genus: Parahaemoproteus was predicted by elevation and climate, Leucocytozoon varied idiosyncratically among mountains, and Plasmodium was unpredictable, but rare. Parasite turnover was nearly three-fold higher than bird turnover and was predicted by elevation, climate, and bird community composition, but not geographic distance. Haemosporidian communities vary strikingly at fine spatial scales (hundreds of kilometers), across which the bird community varies only subtly. The finer scale of turnover among parasites implies that their ranges may be smaller than those of their hosts. Avian host species should encounter different parasite species in different parts of their ranges, resulting in spatially varying selection on host immune systems. The fact that parasite turnover was predicted by bird turnover, even when considering environmental characteristics, implies that host species or their phylogenetic history plays a role in determining which parasite species will be present in a community.

Maladaptive phenotypic plasticity in cardiac muscle growth is suppressed in high-altitude deer mice.

How often phenotypic plasticity acts to promote or inhibit adaptive evolution is an ongoing debate among biologists. Recent work suggests that adaptive phenotypic plasticity promotes evolutionary divergence, though several studies have also suggested that maladaptive plasticity can potentiate adaptation. The role of phenotypic plasticity, adaptive, or maladaptive, in evolutionary divergence remains controversial. We examined the role of plasticity in evolutionary divergence between two species of Peromyscus mice that differ in native elevations. We used cardiac mass as a model phenotype, since ancestral hypoxia-induced responses of the heart may be both adaptive and maladaptive at high-altitude. While left ventricle growth should enhance oxygen delivery to tissues, hypertrophy of the right ventricle can lead to heart failure and death. We compared left- and right-ventricle plasticity in response to hypoxia between captive-bred P. leucopus (representing the ancestral lowland condition) and P. maniculatus from high-altitude. We found that maladaptive ancestral plasticity in right ventricle hypertrophy is reduced in high-altitude deer mice. Analysis of the heart transcriptome suggests that changes in expression of inflammatory signaling genes, particularly interferon regulatory factors, contribute to the suppression of right ventricle hypertrophy. We found weak evidence that adaptive plasticity of left ventricle mass contributes to evolution. Our results suggest that selection to suppress ancestral maladaptive plasticity plays a role in adaptation.

Transcriptomic plasticity in brown adipose tissue contributes to an enhanced capacity for nonshivering thermogenesis in deer mice.

For small mammals living at high altitude, aerobic heat generation (thermogenesis) is essential for survival during prolonged periods of cold, but is severely impaired under conditions of hypobaric hypoxia. Recent studies in deer mice (Peromyscus maniculatus) reveal adaptive enhancement of thermogenesis in high- compared to low-altitude populations under hypoxic cold stress, an enhancement that is attributable to modifications in the aerobic metabolism of muscles used in shivering. However, because small mammals rely heavily on nonshivering mechanisms for cold acclimatization, we tested for evidence of adaptive divergence in nonshivering thermogenesis (NST) under hypoxia. To do so, we measured NST and characterized transcriptional profiles of brown adipose tissue (BAT) in high- and low-altitude deer mice that were (i) wild-caught and acclimatized to their native altitude, and (ii) born and reared under common garden conditions at low elevation. We found that NST performance under hypoxia is enhanced in wild-caught, high-altitude deer mice, a difference that is associated with increased expression of coregulated genes that influence several physiological traits. These traits include vascularization and O2 supply to BAT, brown adipocyte proliferation and the uncoupling of oxidative phosphorylation from ATP synthesis in the generation of heat. Our results suggest that acclimatization to hypoxic cold stress is facilitated by enhancement of nonshivering heat production, which is driven by regulatory plasticity in a suite of genes that influence intersecting physiological pathways.

Intraspecific polymorphism, interspecific divergence, and the origins of function-altering mutations in deer mouse hemoglobin.

Major challenges for illuminating the genetic basis of phenotypic evolution are to identify causative mutations, to quantify their functional effects, to trace their origins as new or preexisting variants, and to assess the manner in which segregating variation is transduced into species differences. Here, we report an experimental analysis of genetic variation in hemoglobin (Hb) function within and among species of Peromyscus mice that are native to different elevations. A multilocus survey of sequence variation in the duplicated HBA and HBB genes in Peromyscus maniculatus revealed that function-altering amino acid variants are widely shared among geographically disparate populations from different elevations, and numerous amino acid polymorphisms are also shared with closely related species. Variation in Hb-O2 affinity within and among populations of P. maniculatus is attributable to numerous amino acid mutations that have individually small effects. One especially surprising feature of the Hb polymorphism in P. maniculatus is that an appreciable fraction of functional standing variation in the two transcriptionally active HBA paralogs is attributable to recurrent gene conversion from a tandemly linked HBA pseudogene. Moreover, transpecific polymorphism in the duplicated HBA genes is not solely attributable to incomplete lineage sorting or introgressive hybridization; instead, it is mainly attributable to recurrent interparalog gene conversion that has occurred independently in different species. Partly as a result of concerted evolution between tandemly duplicated globin genes, the same amino acid changes that contribute to variation in Hb function within P. maniculatus also contribute to divergence in Hb function among different species of Peromyscus. In the case of function-altering Hb mutations in Peromyscus, there is no qualitative or quantitative distinction between segregating variants within species and fixed differences between species.