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Velotta, J. P.

Publications and source records attributed to Velotta, J. P..

5 recordsLinked to original sources

Reduced baseline male fertility and increased sensitivity to hypoxic stress in high-elevation deer mice

Extreme environments like high elevation impose chronic challenges to endothermic animals who must sustain metabolic demand despite reduced oxygen availability. Male reproduction is a tightly regulated physiological system, and hypoxia exposure has negative but transient effects on male reproductive output in diverse mammal species not adapted to high-elevation. Little is known about whether high elevation populations adapt to the detrimental effects of hypoxia on male reproductive physiology. Here, we use high- and low-elevation populations of deer mice (Peromyscus maniculatus) and a lowland congener, P. leucopus, to test how male reproductive phenotypes have diverged across populations and in response to hypoxia exposure across acute, intermediate, and chronic timescales. We complement these phenotypic assays with bulk RNA sequencing of testes to assess the testis-specific response to hypoxia. Contrary to expectations, hypoxia exposure had a negligible effect on low-elevation strains, while highland mice had both lower baseline fertility and heightened sensitivity to hypoxic stress including complete absence of mature sperm. Gene expression patterns indicate that hypoxia exposure dramatically reorganizes testes architecture in highland mice, consistent with testicular regression similar to that observed in seasonally breeding mammals. We hypothesize that this increased sensitivity of male reproductive physiology in highlanders reflects a life history trade-off, allowing energy reallocation between reproduction, survival, and thermogenesis in response to stress in extreme environments.

evolutionary biology↗

Temperature-dependent gene regulatory divergence underlies local adaptation with gene flow in the Atlantic silverside

Gene regulatory divergence is thought to play an important role in adaptation, yet its extent and underlying mechanisms remain largely elusive under scenarios of local adaptation with gene flow. Local adaptation is widespread in marine species despite generally high connectivity and often associated with tightly-linked genomic architectures, such as chromosomal inversions. To investigate gene regulatory evolution under gene flow and the role of discrete genomic regions associated with local adaptation to a steep thermal gradient, we generated RNA-seq data from Atlantic silversides (Menidia menidia) from two locally adapted populations and their F1 hybrids, reared under two different temperatures. We found substantial divergence in gene expression and thermal plasticity, with up to 31% of genes being differentially expressed, and primarily trans-rather than cis-regulatory divergence between populations, despite ongoing gene flow. Substantially reduced thermal plasticity, temperature-dependent gene misexpression and the disruption of co-expression networks in hybrids point toward a role of regulatory incompatibilities in maintaining local adaptation, particularly under colder temperatures, which appear more challenging for this species. Adaptive chromosomal inversions seem to play an important role in gene regulatory divergence through the accumulation of regulatory incompatibilities but are not consistently enriched for divergently regulated genes. Together, these results highlight that gene regulation can diverge substantially among populations connected by strong gene flow in marine environments, partly due to the accumulation of temperature-dependent regulatory incompatibilities within inversions.

evolutionary biology↗

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↗

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↗

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↗