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Comparative Study
. 2019 Jun 1;11(6):1552-1572.
doi: 10.1093/gbe/evz101.

Parallel Molecular Evolution in Pathways, Genes, and Sites in High-Elevation Hummingbirds Revealed by Comparative Transcriptomics

Affiliations
Comparative Study

Parallel Molecular Evolution in Pathways, Genes, and Sites in High-Elevation Hummingbirds Revealed by Comparative Transcriptomics

Marisa C W Lim et al. Genome Biol Evol. .

Abstract

High-elevation organisms experience shared environmental challenges that include low oxygen availability, cold temperatures, and intense ultraviolet radiation. Consequently, repeated evolution of the same genetic mechanisms may occur across high-elevation taxa. To test this prediction, we investigated the extent to which the same biochemical pathways, genes, or sites were subject to parallel molecular evolution for 12 Andean hummingbird species (family: Trochilidae) representing several independent transitions to high elevation across the phylogeny. Across high-elevation species, we discovered parallel evolution for several pathways and genes with evidence of positive selection. In particular, positively selected genes were frequently part of cellular respiration, metabolism, or cell death pathways. To further examine the role of elevation in our analyses, we compared results for low- and high-elevation species and tested different thresholds for defining elevation categories. In analyses with different elevation thresholds, positively selected genes reflected similar functions and pathways, even though there were almost no specific genes in common. For example, EPAS1 (HIF2α), which has been implicated in high-elevation adaptation in other vertebrates, shows a signature of positive selection when high-elevation is defined broadly (>1,500 m), but not when defined narrowly (>2,500 m). Although a few biochemical pathways and genes change predictably as part of hummingbird adaptation to high-elevation conditions, independent lineages have rarely adapted via the same substitutions.

Keywords: Andes; Trochilidae; convergent evolution; hypoxia; respiratory electron transport; transcriptome.

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Figures

<sc>Fig</sc>. 1.
Fig. 1.
—(A) Elevation ranges (black lines), midpoint elevations, and specimen sampling elevations for the 12 study species (A, Phaethornis malaris; B, Colibri coruscans; C, Aglaeactis castelnaudii; D, Coeligena coeligena; E, Coeligena violifer; F, Phlogophilus harterti; G, Adelomyia melanogenys; H, Metallura phoebe; I, Patagona gigas peruviana; J, Chaetocercus mulsant; K, Amazilia amazilia; and L, Amazilia viridicauda). We used specimen data, expert knowledge, and Schulenberg et al. (2007) to identify the core elevational ranges of each sampled taxon in our study. Hummingbird illustrations are from del Hoyo et al. (2018). (B) Gray bars mark species groups for the four elevation scenarios to test for high-altitude adaptation in species with midpoint elevations occurring >2,500 m (Test 1), <1,500 m (Test 2), >1,500 m (Test 1a), and <2,500 m (Test 2a). (C) Phylogenetic relationships between study species pruned from McGuire et al. (2014).
<sc>Fig</sc>. 2.
Fig. 2.
—Diagram of the subset of PSGs that are involved with cellular respiration in (A) the Krebs cycle or (B) the oxidative phosphorylation pathway. We used information from the Genecards and KEGG databases to identify the location where PSG gene products act within the pathways. The font color and symbols (*, +, and −) for PSGs indicate the elevation category of the species for which the gene was identified. PSG results from the multibranch foreground PAML analyses are indicated in bold text.

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