skip to main content

Explore Research Products in the NSF-PAR

Title: The genomic basis of high-elevation adaptation in wild house mice ( Mus musculus domesticus ) from South America
Abstract

Understanding the genetic basis of environmental adaptation in natural populations is a central goal in evolutionary biology. The conditions at high elevation, particularly the low oxygen available in the ambient air, impose a significant and chronic environmental challenge to metabolically active animals with lowland ancestry. To understand the process of adaptation to these novel conditions and to assess the repeatability of evolution over short timescales, we examined the signature of selection from complete exome sequences of house mice (Mus musculus domesticus) sampled across two elevational transects in the Andes of South America. Using phylogenetic analysis, we show that house mice colonized high elevations independently in Ecuador and Bolivia. Overall, we found distinct responses to selection in each transect and largely nonoverlapping sets of candidate genes, consistent with the complex nature of traits that underlie adaptation to low oxygen availability (hypoxia) in other species. Nonetheless, we also identified a small subset of the genome that appears to be under parallel selection at the gene and SNP levels. In particular, three genes (Col22a1, Fgf14, and srGAP1) bore strong signatures of selection in both transects. Finally, we observed several patterns that were common to both transects, including an excess of derived alleles at high elevation, and a number of hypoxia-associated genes exhibiting a threshold effect, with a large allele frequency change only at the highest elevations. This threshold effect suggests that selection pressures may increase disproportionately at high elevations in mammals, consistent with observations of some high-elevation diseases in humans.

  more » « less
NSF-PAR ID:
10385159
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
Genetics
Volume:
220
Issue:
2
ISSN:
1943-2631
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; ( , Insect Systematics and Diversity)
    Ware, Jessica (Ed.)
    Abstract Broadly distributed species experience divergent abiotic conditions across their ranges that may drive local adaptation. Montane systems where populations are distributed across both latitudinal and elevational gradients are especially likely to produce local adaptation due to spatial variation in multiple abiotic factors, including temperature, oxygen availability, and air density. We use whole-genome resequencing to evaluate the landscape genomics of Bombus vancouverensis Cresson (Hymenoptera: Apidae), a common montane bumble bee that is distributed throughout the western part of North America. Combined statistical approaches revealed several large windows of outlier SNPs with unusual levels of differentiation across the region and indicated that isothermality and elevation were the environmental features most strongly associated with these variants. Genes found within these regions had diverse biological functions, but included neuromuscular function, ion homeostasis, oxidative stress, and hypoxia that could be associated with tolerance of temperature, desiccation, or high elevation conditions. The whole-genome sequencing approach revealed outliers occurred in genome regions with elevated linkage disequilibrium, elevated mean FST, and low intrapopulation nucleotide diversity. Other kinds of structural variations were not widely associated with environmental predictors but did broadly match geographic separation. Results are consistent with other studies suggesting that regions of low recombination may harbor adaptive variation in bumble bees within as well as between species and refine our understanding of candidate genes that could be further investigated as possible targets of selection across the B. vancouverensis range. 
    more » « less
  2. ; ; ; ; ; ; ( , Functional Ecology)
    Abstract

    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 VO2maxmeasures 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.

    Aplain language summaryis available for this article.

     
    more » « less
  3. ; ; ; ; ; ( , Biology Letters)
    Animals developing at high elevation experience a suite of environmental challenges, most notably the low partial pressure of oxygen ( P O 2 ) in ambient air. In low P O 2 , bird species with high-elevation ancestry consistently demonstrate higher hatching success than lowland counterparts, suggesting highland birds are adapted to restricted O 2 (hypoxia) in early development. Haemoglobin (Hb), the critical oxygen-transport protein, is a likely target of P O 2 -related selection across ontogeny since Hb isoforms expressed at distinct developmental stages demonstrate different O 2 affinities. To test if Hb function is under P O 2 -related selection at different ontogenetic stages, we sampled a songbird, the hooded siskin ( Spinus magellanicus ), across two approximately 4000 m elevational transects. We sequenced all of the loci that encode avian Hb isoforms, and tested for signatures of spatially varying selection by comparing divergence patterns in Hb loci to other loci sampled across the genome. We found strong signatures of diversifying selection at non-synonymous sites in loci that contribute to embryonic ( α π , β H ) and definitive ( β A ) Hb isoforms. This is the first evidence for selection on embryonic haemoglobin in high-elevation Neoaves. We conclude that selection on Hb function at brief, but critical stages of ontogeny may be a vital component to high elevation adaptation in birds. 
    more » « less
  4. ; ; ; ; ( , Journal of Heredity)
    Chapman, Mark (Ed.)
    Abstract Populations along steep environmental gradients are subject to differentiating selection that can result in local adaptation, despite countervailing gene flow, and genetic drift. In montane systems, where species are often restricted to narrow ranges of elevation, it is unclear whether the selection is strong enough to influence functional differentiation of subpopulations differing by a few hundred meters in elevation. We used targeted capture of 12 501 exons from across the genome, including 271 genes previously implicated in altitude adaptation, to test for adaptation to local elevations for 2 highland hummingbird species, Coeligena violifer (n = 62) and Colibri coruscans (n = 101). For each species, we described population genetic structure across the complex geography of the Peruvian Andes and, while accounting for this structure, we tested whether elevational allele frequency clines in single nucleotide polymorphisms (SNPs) showed evidence for local adaptation to elevation. Although the 2 species exhibited contrasting population genetic structures, we found signatures of clinal genetic variation with shifts in elevation in both. The genes with SNP-elevation associations included candidate genes previously discovered for high-elevation adaptation as well as others not previously identified, with cellular functions related to hypoxia response, energy metabolism, and immune function, among others. Despite the homogenizing effects of gene flow and genetic drift, natural selection on parts of the genome evidently optimizes elevation-specific cellular function even within elevation range-restricted montane populations. Consequently, our results suggest local adaptation occurring in narrow elevation bands in tropical mountains, such as the Andes, may effectively make them “taller” biogeographic barriers. 
    more » « less
  5. ; ; ; ; ; ( , Proceedings of the National Academy of Sciences)

    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 gestational parent and fetus. We then use compartment-specific 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 candidate 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.

     
    more » « less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email