Biology subjects

Cheviron, Z. A.

Publications and source records attributed to Cheviron, Z. A..

14 recordsLinked to original sources

bioRxiv2025

Elevational variation in heart mass and suppression of hypoxia-induced right ventricle hypertrophy in Andean leaf-eared mice (Phyllotis)

In lowland mammals that ascend to high elevation, hypoxia-induced changes in the pulmonary circulation can give rise to hypoxic pulmonary hypertension (HPH) and associated right-ventricle (RV) hypertrophy. Some mammals that are native to high elevation have evolved a means of attenuating HPH, demonstrating how environmental adaptation may sometimes counteract the effects of ancestral acclimatization responses. Here, we examine elevational variation in heart mass and measures of RV hypertrophy in four closely related species of leaf-eared mice (genus Phyllotis) that are broadly co-distributed across a steep elevational gradient on the Western slope of the Andes. There was a positive relationship overall between heart mass and elevation that reflected proportional changes in both the right and left ventricles. Thus, elevation-related increases in overall heart mass were not generally attributable to RV hypertrophy, suggesting that this group of predominantly highland species have evolved a means of avoiding HPH and/or attenuating the cardiac response to HPH. To gain insight into possible transcriptional mechanisms, we examined patterns of transcriptomic variation in the right ventricles of Phyllotis vaccarum from two geographically distinct highland populations (both from elevations >5000 m) that exhibit strikingly different levels of RV hypertrophy. Suppression of RV hypertrophy is associated with differential expression of key regulatory genes involved in striated muscle, immune processes, and the inflammatory response. Analysis of co-expression modules identified a promising set of candidate genes for mediating the development of RV hypertrophy at extremely high elevations.

evolutionary biology↗

bioRxiv2024

Species limits and hybridization in Andean leaf-eared mice (Phyllotis)

Leaf-eared mice (genus Phyllotis) are among the most widespread and abundant small mammals in the Andean Altiplano, but species boundaries and distributional limits are often poorly delineated due to sparse survey data from remote mountains and high-elevation deserts. Here we report a combined analysis of mitochondrial DNA variation and whole-genome sequence (WGS) variation in Phyllotis mice to delimit species boundaries, to assess the timescale of diversification of the group, and to examine evidence for interspecific hybridization. Estimates of divergence dates suggest that most diversification of Phyllotis occurred during the past 3 million years. Consistent with the Pleistocene Aridification hypothesis, our results suggest that diversification of Phyllotis largely coincided with climatically induced environmental changes in the mid- to late Pleistocene. Contrary to the Montane Uplift hypothesis, most diversification in the group occurred well after the major phase of uplift of the Central Andean Plateau. Species delimitation analyses revealed surprising patterns of cryptic diversity within several nominal forms, suggesting the presence of much undescribed alpha diversity in the genus. Results of genomic analyses revealed evidence of ongoing hybridization between the sister species Phyllotis limatus and P. vaccarum and suggest that the contemporary zone of range overlap between the two species represents an active hybrid zone.

evolutionary biology↗

bioRxiv2024

Local adaptation, plasticity, and evolved resistance to hypoxic cold stress in high-altitude deer mice

A fundamental question in evolutionary biology concerns the relative contributions of phenotypic plasticity vs. local adaptation (genotypic specialization) in enabling wide-ranging species to inhabit diverse environmental conditions. Here we conduct a long-term hypoxia acclimation experiment to assess the relative roles of local adaptation and plasticity in enabling highland and lowland deer mice (Peromyscus maniculatus) to sustain aerobic thermogenesis at progressively increasing elevations. We assessed the relative physiological performance capacities of highland and lowland natives as they were exposed to progressive, stepwise increases in hypoxia, simulating the gradual ascent from sea level to an elevation of 6000 m. The final elevation of 6000 m far exceeds the highest attainable elevations within the species range, and therefore tests the animals ability to tolerate levels of hypoxia that surpass the prevailing conditions within their current distributional limits. Our results demonstrate that highland natives exhibit superior thermogenic capacities at the most severe levels of hypoxia, suggesting that the species broad fundamental niche and its ability to inhabit such a broad range of elevational zones is attributable to a combination of genetically based local adaptation and plasticity. Transcriptomic and physiological measurements identify evolved changes in the acclimation response to hypoxia that contribute to the enhanced thermogenic capacity of highland natives. SIGNIFICANCE STATEMENTIn species that are distributed across steep environmental gradients, the ability to inhabit a broad range of conditions may be attributable to local adaptation and/or a generalized acclimatization capacity (phenotypic plasticity). By experimentally acclimating highland and lowland deer mice (Peromyscus maniculatus) to progressively increasing levels of hypoxia during a simulated ascent to 6000 m, we assessed the relative roles of evolved and plastic changes in thermogenic capacity. At especially severe levels of hypoxia, the superior thermogenic performance of highland natives relative to lowland conspecifics suggests that the broad fundamental niche of deer mice is largely attributable to local adaptation to different elevational zones, including evolved plasticity in gene expression and respiratory traits.

evolutionary biology↗

bioRxiv2022

Thermal acclimation in a non-migratory songbird occurs via changes to thermogenic capacity, but not conductance

Thermoregulatory performance can be modified through changes in various subordinate traits, including thermal conductance, basal and summit metabolic rates, and body composition. We investigated physiological differences between black-capped chickadees (Poecile atricapillus) acclimated for six weeks to cold (-5{degrees}C) or control (25{degrees}C) environments (n = 7 per treatment) by measuring traits that affect thermal balance. We made repeated measurements of basal and summit metabolic rates via flow-through respirometry and body composition using quantitative magnetic resonance of live birds. At the end of the acclimation, we measured thermal conductance of the combined feathers and skins. Cold-acclimated birds had a higher summit metabolic rate, reflecting a greater capacity for endogenous heat generation, and an increased lean mass. However, birds did not alter their thermal conductance. These results suggest that, while birds can use multiple mechanisms to acclimate to their thermal environment, they use a subset of potential changes over varying timescales.

physiology↗

bioRxiv2022

Adaptive structural and functional evolution of the placenta protects fetal growth in high elevation deer mice

Environmental hypoxia challenges female reproductive physiology in placental mammals, increasing rates of gestational complications. Adaptation to high elevation has limited many of these effects in humans and other mammals, offering potential insight into the developmental processes that lead to and protect against hypoxia-related gestational complications. However, our understanding of these adaptations has been hampered by a lack of experimental work linking the functional, regulatory, and genetic underpinnings of gestational development in locally-adapted populations. Here, we dissect high-elevation adaptation in the reproductive physiology of deer mice, (Peromyscus maniculatus), a rodent species with an exceptionally broad elevational distribution that has emerged as a model for hypoxia adaptation. Using experimental acclimations, we show that lowland mice experience pronounced fetal growth restriction when challenged with gestational hypoxia, while highland mice maintain normal growth by expanding the compartment of the placenta that facilitates nutrient and gas exchange between dam and fetus. We then use compartmentspecific transcriptome analyses to show that adaptive structural remodeling of the placenta is coincident with widespread changes in gene expression within this same compartment. Genes associated with fetal growth in deer mice significantly overlap with genes involved in human placental development, pointing to conserved or convergent pathways underlying these processes. Finally, we overlay our results with genetic data from natural populations to identify can-didate genes and genomic features that contribute to these placental adaptations. Collectively, these experiments advance our understanding of adaptation to hypoxic environments by revealing physiological and genetic mechanisms that shape fetal growth trajectories under maternal hypoxia. Significance StatementResidence at high elevations is associated with higher risk pregnancies and low birth weight, yet the causal mechanisms remain poorly understood. Using a high elevation-adapted rodent model, we investigated the physiological traits that explain fetal growth trajectories in low oxygen environments, and how evolutionary adaptation has modified these traits. We showed that high- and low-elevation populations of deer mice differ in their susceptibility to fetal growth restriction during gestational hypoxia and that these population-level differences are associated with structural and transcriptomic changes in the placenta. We further link placental gene expression to genomic features under selection at high elevation. Our findings identify adaptations that are likely relevant to offsetting the effects of hypoxia on fetal and placental development across mammals.

evolutionary biology↗

bioRxiv2022

Gene regulatory changes underlie developmental plasticity in respiration and aerobic performance in highland deer mice

Phenotypic plasticity can play an important role in the ability of animals to tolerate environmental stress, but the nature and magnitude of plastic responses are often specific to the developmental timing of exposure. Here, we examine changes in gene expression in the diaphragm of highland deer mice (Peromyscus maniculatus) in response to hypoxia exposure at different stages of development. In highland deer mice, developmental plasticity in diaphragm function may mediate changes in several respiratory traits that influence aerobic metabolism and performance under hypoxia. We generated RNAseq data from diaphragm tissue of adult deer mice exposed to 1) life-long hypoxia (before conception to adulthood), 2) post-natal hypoxia (birth to adulthood), 3) adult hypoxia (6-8 weeks only during adulthood), or 4) normoxia. We found five suites of co-regulated genes that are differentially expressed in response to hypoxia, but the patterns of differential expression depend on the developmental timing of exposure. We also identified four transcriptional modules that are associated with important respiratory traits. Many of the genes in these transcriptional modules bear signatures of altitude-related selection, providing an indirect line of evidence that observed changes in gene expression may be adaptive in hypoxic environments. Our results demonstrate the importance of developmental stage in determining the phenotypic response to environmental stressors.

molecular biology↗

bioRxiv2021

The architecture of phenotypic flexibility within a complex trait: an empirical case study using avian thermogenic performance

Reversible modifications to trait values can allow individuals to match their phenotypes to changing environmental conditions, a phenomenon known as phenotypic flexibility. A systems capacity for flexibility may be determined by its underlying architecture, and these relationships can have important implications for both organismal adaptation and the evolvability of acclimatization responses. Theory provides two possible alternatives to explain the ways in which lower-level traits respond to environmental challenges and contribute to phenotypic flexibility in complex, whole-organism traits: symmorphosis predicts correspondence between structure and demand across all levels of a physiological system, while the alternative predicts that influence is concentrated in select elements of a physiological network. Here we provide a rich dataset -- composed of 20 sub-organismal, physiological traits paired with whole-organism metabolic rates for 106 adult Dark-eyed Juncos (Junco hyemalis) -- to explore the mechanistic basis of phenotypic flexibility in complex traits. When exposed to synthetic temperature cues, these individuals have previously been shown to increase their thermogenic capacity (Msum) and enhance their ability to maintain their body temperature in the cold. We show that the relationships among a number of the traits that contribute to Msum varied as the environmental context changed. Moreover, variation in Msum in response to temperature acclimation was correlated with only a handful of subordinate phenotypes. As a result, avian thermogenic flexibility does not appear to be a symmorphotic response. If this is generally true of complex traits, it suggests that simple and reversible modifications can significantly impact whole-organism performance, and thus that the evolution of phenotypic flexibility in a single component part could impart flexibility for the entire system.

evolutionary biology↗

bioRxiv2021

Haemosporidian infection does not alter aerobic performance in the Pink-sided Junco (Junco hyemalis mearnsi)

Avian haemosporidia are blood parasites that can have dramatic fitness consequences on their hosts, including largescale population declines when introduced to naive hosts. Yet the physiological effects that accompany haemosporidian infection and underlie these fitness decrements are poorly characterized in most wild birds. Because haemosporidia destroy host red blood cells and consume host hemoglobin, they are predicted to have detrimental impacts on avian blood-oxygen transport and, as a result, reduce aerobic performance. However, the documented effects of infection on avian hematological traits vary across species and no effects have been demonstrated on avian aerobic performance to date. Here we quantified the physiological effects of haemosporidian infections on wild Pink-sided Juncos (Junco hyemalis mearnsi) breeding in northwestern Wyoming, USA. We assayed hematological traits (hemoglobin concentration and hematocrit) and aerobic performance (resting and summit metabolic rates, thermogenic endurance, and aerobic scope), then screened individuals for haemosporidian infection post-hoc (n = 106 adult juncos). We found that infection status did not correlate with any of the physiological indices that we measured, suggesting there is little cost of haemosporidian infection on either junco aerobic performance or energy budgets. Our results highlight the need for more studies of haemosporidia infections in a broader range of species and in a wider array of environmental contexts.

physiology↗

bioRxiv2021

Genetic variation in haemoglobin regulates breathing in high-altitude deer mice

Physiological systems often have emergent properties but the effects of genetic variation on physiology are often unknown, which presents a major challenge to understanding the mechanisms of phenotypic evolution. We investigated the in vivo effects on respiratory physiology of genetic variants in haemoglobin (Hb) that contribute to hypoxia adaptation in high-altitude deer mice (Peromyscus maniculatus). We created F2 inter-population hybrids of highland and lowland deer mice to test the phenotypic effects of - and {beta}-globin variants on a mixed genetic background. High-altitude genotypes were associated with breathing phenotypes that enhance O2 uptake in hypoxia, including a deeper more effective breathing pattern and an augmented hypoxic ventilatory response. These effects could not be explained by erythrocyte Hb-O2 affinity or globin gene expression in the brainstem. Therefore, adaptive variation in haemoglobin can have unexpected effects on physiology that are distinct from the canonical function of this protein in circulatory O2 transport.

evolutionary biology↗

bioRxiv2020

Temperature heterogeneity correlates with intraspecific variation in physiological flexibility in a small endotherm

Phenotypic flexibility allows individuals to reversibly modify trait values and theory predicts an individuals relative degree of flexibility positively correlates with the environmental heterogeneity it experiences. We tested this prediction by integrating surveys of population genetic and physiological variation with thermal acclimation experiments and indices of environmental heterogeneity in the Dark-eyed Junco (Junco hyemalis) and its congeners. We combined measures of thermogenic capacity for ~300 individuals, >21,000 single nucleotide polymorphisms genotyped in 192 individuals, and laboratory acclimations replicated on five populations. We found that Junco populations: (1) differ in their thermal performance responses to temperature variation in situ; (2) exhibit intra-specific variation in their thermogenic flexibility in the laboratory that correlates with heterogeneity in their native thermal environment; and (3) harbor genetic variation that also correlates with temperature heterogeneity. These results provide comprehensive support that phenotypic flexibility corresponds with environmental heterogeneity and highlight its importance for coping with environmental change.

evolutionary biology↗

bioRxiv2020

The adaptive benefit of increases in hemoglobin-O2 affinity is contingent on tissue O2 diffusing capacity in high-altitude deer mice

BackgroundComplex organismal traits are often the result of multiple interacting genes and sub-organismal phenotypes, but how these interactions shape the evolutionary trajectories of adaptive traits is poorly understood. We examined how functional interactions between cardiorespiratory traits contribute to adaptive increases in the capacity for aerobic thermogenesis (maximal O2 consumption, V{square}O2max, during acute cold exposure) in high-altitude deer mice (Peromyscus maniculatus). We crossed highland and lowland deer mice to produce F2 inter-population hybrids, which expressed genetically based variation in hemoglobin (Hb) O2 affinity on a mixed genetic background. We then combined physiological experiments and mathematical modeling of the O2 transport pathway to examine links between cardiorespiratory traits and V{square}O2max. ResultsPhysiological experiments revealed that increases in Hb-O2 affinity of red blood cells improved blood oxygenation in hypoxia, but were not associated with an enhancement in V{square}O2max. Sensitivity analyses performed using mathematical modeling showed that the influence of Hb-O2 affinity on V{square}O2max in hypoxia was contingent on the capacity for O2 diffusion in active tissues. ConclusionsThese results suggest that increases in Hb-O2 affinity would only have adaptive value in hypoxic conditions if concurrent with or preceded by increases in tissue O2 diffusing capacity. In high-altitude deer mice, the adaptive benefit of increasing Hb-O2 affinity is contingent on the capacity to extract O2 from the blood, which helps resolve controversies about the general role of hemoglobin function in hypoxia tolerance.

physiology↗

bioRxiv2020

X chromosome-dependent disruption of placental regulatory networks in hybrid dwarf hamsters

Embryonic development in mammals is highly sensitive to changes in gene expression within the placenta. The placenta is also highly enriched for genes showing parent-of-origin or imprinted expression, which is predicted to evolve rapidly in response to parental conflict. However, little is known about the evolution of placental gene expression, or if divergence of placental gene expression plays an important role in mammalian speciation. We used crosses between two species of dwarf hamsters (Phodopus sungorus and P. campbelli) to examine the genetic and regulatory underpinnings of severe placental overgrowth in their hybrids. Using quantitative genetic mapping and mitochondrial substitution lines, we show that overgrowth of hybrid placentas was primarily caused by genetic differences on the maternally inherited P. sungorus X chromosome. Mitochondrial interactions did not contribute to abnormal hybrid placental development, and there was only weak correspondence between placental disruption and embryonic growth. Genome-wide analyses of placental transcriptomes from the parental species and first and second-generation hybrids revealed a central group of co-expressed X-linked and autosomal genes that were highly enriched for maternally-biased expression. Expression of this gene network was strongly correlated with placental size and showed widespread misexpression dependent on epistatic interactions with X-linked hybrid incompatibilities. Collectively, our results indicate that the X chromosome is likely to play a prominent role in the evolution of placental gene expression and the accumulation of hybrid developmental barriers between mammalian species.

evolutionary biology↗

bioRxiv2020

Body temperature maintenance acclimates in a winter-tenacious songbird

Flexibility in heat generation and dissipation mechanisms provides endotherms the ability to match their thermoregulatory strategy with external demands. However, the degree to which these two mechanisms account for seasonal changes in body temperature regulation is unexplored. Here we present novel data on the regulation of avian body temperature to investigate how birds alter mechanisms of heat production and heat conservation to deal with variation in ambient conditions. We subjected Dark-eyed Juncos (Junco hyemalis) to chronic cold acclimations of varying duration and subsequently quantified their metabolic rates, thermal conductance, and ability to maintain normothermia. Cold-acclimated birds adjusted traits related to both heat generation (increased summit metabolic rate) and heat conservation (decreased conductance) to improve their body temperature regulation. Increases in summit metabolic rate occurred rapidly, but plateaued after one week of cold exposure. In contrast, changes to conductance occurred only after nine weeks of cold exposure. Thus, the ability to maintain body temperature continued to improve throughout the experiment, but the mechanisms underlying this improvement changed through time. Our results demonstrate the ability of birds to adjust thermoregulatory strategies in response to thermal cues and reveal that birds may combine multiple responses to meet the specific demands of their environments.

physiology↗

bioRxiv2019

Adaptive shifts in gene regulation underlie a developmental delay in thermogenesis in high-altitude deer mice

Aerobic performance is tied to fitness as it influences an animals ability to find food, escape predators, or survive extreme conditions. At high altitude, where low O2 availability and persistent cold prevail, maximum metabolic heat production (thermogenesis) is an aerobic performance trait that is intimately linked to survival. Understanding how thermogenesis evolves to enhance survival at high altitude will yield insight into the links between physiology, performance, and fitness. Recent work in deer mice (Peromyscus maniculatus) has shown that adult mice native to high-altitude have higher thermogenic capacities under hypoxia compared to lowland conspecifics, but developing high-altitude pups delay the onset of thermogenesis. This suggests that natural selection on thermogenic capacity varies across life stages. To determine the mechanistic cause of this ontogenetic delay, we analyzed the transcriptomes of thermo-effector organs - brown adipose tissue and skeletal muscle - in developing deer mice native to low- and high-altitude. We demonstrate that the developmental delay in thermogenesis is associated with adaptive shifts in the expression of genes involved in nervous system development, fuel/O2 supply, and oxidative metabolism gene pathways. Our results demonstrate that selection has modified the developmental trajectory of the thermoregulatory system at high altitude and has done so by acting on the regulatory systems that control the maturation of thermo-effector tissues. We suggest that the cold and hypoxic conditions of high altitude may force a resource allocation trade-off, whereby limited energy is allocated to developmental processes such as growth, versus active thermogenesis during early development.

evolutionary biology↗