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.
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.
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.
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 4000 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 down-slope 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.
Elevations >2,000 m represent consistently harsh environments for small endotherms because of abiotic stressors such as cold temperatures and hypoxia. These environmental stressors may limit the ability of populations living at these elevations to respond to biotic selection pressures—such as parasites or pathogens—that in other environmental contexts would impose only minimal energetic‐ and fitness‐related costs. We studied deer mice (Peromyscus maniculatus rufinus) living along two elevational transects (2,300–4,400 m) in the Colorado Rockies and found that infection prevalence by botfly larvae (Cuterebridae) declined at higher elevations. We found no evidence of infections at elevations >2,400 m, but that 33.6% of all deer mice, and 52.2% of adults, were infected at elevations <2,400 m. Botfly infections were associated with reductions in haematocrit levels of 23%, haemoglobin concentrations of 27% and cold‐induced VO2max measures of 19% compared to uninfected individuals. In turn, these reductions in aerobic performance appeared to influence fitness, as infected individuals exhibited 19‐34% lower daily survival rates. In contrast to studies at lower elevations, we found evidence indicating that botfly infections influence the aerobic capabilities and fitness of deer mice living at elevations between 2,000 and 2,400 m. Our results therefore suggest that the interaction between botflies and small rodents is likely highly context‐dependent and that, more generally, high‐elevation populations may be susceptible to additional biotic selection pressures. A plain language summary is available for this article.
23 1. Haemosporidian parasites of birds are ubiquitous in terrestrial ecosystems, but their 24 coevolutionary dynamics remain poorly understood. If species turnover in parasites occurs at a 25 finer scale than species turnover in hosts, widespread hosts would encounter diverse parasites 26 and potentially diversify as a result. Previous studies have shown that some wide-ranging hosts 27 encounter varied haemosporidian communities throughout their range, and vice-versa. However, 28it remains difficult to test spatial patterns of diversity in this complex multi-host multi-parasite 29 system because it remains inadequately surveyed. 30 2. We sought to understand how and why a community of avian haemosporidian parasites varies 31 in abundance and composition across an array of eight sky islands in southwestern North 32America. We tested whether bird community composition, aspects of the environment, or 33 geographic distance explain parasite species turnover in a widespread, generalist host. 34 3. We sampled 178 Audubon's Warblers (Setophaga auduboni) along elevational transects in 35 eight mountain ranges and screened them for haemosporidian mtDNA. We tested predictors of 36 infection using generalized linear models (GLMs) and we tested predictors of bird-and parasite-37 community dissimilarity using generalized dissimilarity modeling (GDM). 38 4. Predictors of infection differed by genus: Parahaemoproteus was predicted by elevation and 39 climate, Leucocytozoon varied idiosyncratically among mountain ranges, and Plasmodium was 40 unpredictable, but rare. Parasite species turnover was nearly three-fold higher than bird species 41 turnover and was predicted by elevation, climate, and bird community composition, but not by 42 geographic distance. 43 5. Haemosporidian communities vary strikingly at spatial scales of hundreds of kilometers, 44 across which the bird community varies only subtly. The finer spatial scale of turnover among 45 Ecology explains sky-island parasite communities 3 parasites species implies that their ranges tend to be smaller than those of their hosts. Avian host 46 species should encounter different parasite species in different parts of their ranges, resulting in 47
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