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

Abstract

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 interferonregulatory 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.

Transplanting gravid lizards to high elevation alters maternal and embryonic oxygen physiology, but not reproductive success or hatchling phenotype

“…As has been found in previous studies of transplanted lizards (He et al, 2013;Gangloff et al, 2019;Weathers and McGrath, 1972) we predicted physiological plasticity in parameters related to oxygen-carrying capacity in blood chemistry (haematocrit and haemoglobin concentration) in reproductive females from low elevations transplanted to high elevations. Importantly, we did not expect the physiological profile of lowland lizards transplanted to high elevation to match those of lizards from high-elevation populations, as often the short-term plastic response differs from that of locally adapted populations (He et al, 2013;Jochmans-Lemoine et al, 2015;Reyes et al, 2018;Storz et al, 2010;Velotta et al, 2018). We predicted that such shifts in oxygen capacity would allow lizards to maintain resting metabolic rates but perhaps bear other physiological or reproductive consequences given the increased energetic demands of reproduction (Angilletta and Sears, 2000;Foucart et al, 2014).…”

Development of homeothermic endothermy is delayed in high-altitude native deer mice ( Peromyscus maniculatus)

“…Instead, we suggest this delay is a cost-saving adaptation that allows HA pups to maintain growth rates under the O 2 -limited conditions. This seemingly paradoxical result is at odds with the elevated thermogenic capacity seen in adult HA mice [28,29], which improves overwinter survival and is under directional selection at HA [31]. Our findings stress the importance of understanding how the same selective pressures can act differently depending on life-history stage to truly understand the evolution of an adaptive physiological trait.…”

“…If HA pups are nutrient limited owing to increased competition from litter mates, then suppressing energetically costly thermogenesis may help them recoup some of their energetic costs in favour of maintaining growth rates even in normoxia. This may also allow the preservation of BAT for adulthood, when it is probably critical for re-warming from bouts of torpor [30,31].…”

UNVEILing connections between genotype, phenotype, and fitness in natural populations

“…At high altitude (>4,000 m above sea level), however, chronically elevated erythropoiesis driven by environmental hypoxia can cause hypertension and cardiac hypertrophy, both of which are associated with high‐altitude diseases in lowlanders. Velotta found that high‐altitude deer mice have evolved to suppress the erythropoietic response to hypoxia, which is likely adaptive over the long term under the chronically hypoxic conditions experienced at altitude (Velotta, Ivy, Wolf, Scott, & Cheviron, ). They suspect that this suppression is the result of compensatory evolution, and not the result of selection directly on the genes involved in erythropoiesis; it is indeed likely that evolution to suppress maladaptive plasticity may in general be achieved by compensatory changes that protect an organism's internal homeostatic environment against perturbations from the external environment (Velotta & Cheviron, ).…”