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Local adaptation to altitude underlies divergent thermal physiology in tropical killifishes of the genus Aphyosemion.

ABSTRACT: In watersheds of equatorial West Africa, monophyletic groups of killifish species (genus Aphyosemion) occur in discrete altitudinal ranges, low altitude species (LA, sea level to ∼350 m) or high altitude species (HA, 350 to 900 m). We investigated the hypothesis that local adaptation to altitude by the LA and HA species would be revealed as divergent effects of temperature on their physiological energetics. Two species from each group (mass ∼350 mg) were acclimated to 19, 25 and 28°C, with 19 and 28°C estimated to be outside the thermal envelope for LA or HA, respectively, in the wild. Wild-caught animals (F0 generation) were compared with animals raised in captivity at 25°C (F1 generation) to investigate the contribution of adaptation versus plasticity. Temperature significantly increased routine metabolic rate in all groups and generations. However, LA and HA species differed in the effects of temperature on their ability to process a meal. At 25°C, the specific dynamic action (SDA) response was completed within 8 h in all groups, but acclimation to temperatures beyond the thermal envelope caused profound declines in SDA performance. At 19°C, the LA required ∼14 h to complete the SDA, whereas the HA required only ∼7 h. The opposite effect was observed at 28°C. This effect was evident in both F0 and F1. Reaction norms for effects of temperature on SDA therefore revealed a trade-off, with superior performance at warmer temperatures by LA being associated with inferior performance at cooler temperatures, and vice-versa in HA. The data indicate that divergent physiological responses to temperature in the LA and HA species reflect local adaptation to the thermal regime in their habitat, and that local adaptation to one thermal environment trades off against performance in another.

SUBMITTER: McKenzie DJ

PROVIDER: S-EPMC3551936 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:High altitudes (>8,000 ft or 2,500 m) provide an experiment of nature for measuring adaptation and the physiological processes involved. Studies conducted over the past ~25 years in Andeans, Tibetans, and, less often, Ethiopians show varied but distinct O2 transport traits from those of acclimatized newcomers, providing indirect evidence for genetic adaptation to high altitude. Short-term (acclimatization, developmental) and long-term (genetic) responses to high altitude exhibit a temporal gradient such that, although all influence O2 content, the latter also improve O2 delivery and metabolism. Much has been learned concerning the underlying physiological processes, but additional studies are needed on the regulation of blood flow and O2 utilization. Direct evidence of genetic adaptation comes from single-nucleotide polymorphism (SNP)-based genome scans and whole genome sequencing studies that have identified gene regions acted upon by natural selection. Efforts have begun to understand the connections between the two with Andean studies on the genetic factors raising uterine blood flow, fetal growth, and susceptibility to Chronic Mountain Sickness and Tibetan studies on genes serving to lower hemoglobin and pulmonary arterial pressure. Critical for future studies will be the selection of phenotypes with demonstrable effects on reproductive success, the calculation of actual fitness costs, and greater inclusion of women among the subjects being studied. The well-characterized nature of the O2 transport system, the presence of multiple long-resident populations, and relevance for understanding hypoxic disorders in all persons underscore the importance of understanding how evolutionary adaptation to high altitude has occurred.NEW & NOTEWORTHY Variation in O2 transport characteristics among Andean, Tibetan, and, when available, Ethiopian high-altitude residents supports the existence of genetic adaptations that improve the distribution of blood flow to vital organs and the efficiency of O2 utilization. Genome scans and whole genome sequencing studies implicate a broad range of gene regions. Future studies are needed using phenotypes of clear relevance for reproductive success for determining the mechanisms by which naturally selected genes are acting.

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Local adaptation to altitude underlies divergent thermal physiology in tropical killifishes of the genus Aphyosemion.

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