TY - JOUR
T1 - Ontogenesis of evolved changes in respiratory physiology in deer mice native to high altitude
AU - Ivy, Catherine M.
AU - Greaves, Mary A.
AU - Sangster, Elizabeth D.
AU - Robertson, Cayleih E.
AU - Natarajan, Chandrasekhar
AU - Storz, Jay F.
AU - McClelland, Grant B.
AU - Scott, Graham R.
N1 - Funding Information:
C.M.I. was supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) PGS-D and Ontario Graduate Scholarship; C.E.R. was supported by a Natural Sciences and Engineering Research Council of Canada CGS-D grant; J.F.S. was supported by grants from the National Institutes of Health (HL087216) and the National Science Foundation (OIA-1736249 and IOS-1927675); G.B.M. was supported by a Natural Sciences and Engineering Research Council of Canada Discovery Grant and a Natural Sciences and Engineering Research Council of Canada Discovery Accelerator Supplement; G.R.S. was supported by a Natural Sciences and Engineering Research Council of Canada Discovery Grant and Canada Research Chairs program. Deposited in PMC for release after 12 months.
Funding Information:
We would like to thank Dr Colin Nurse for his insight and for allowing us to use his microscope for carotid body imaging. C.M.I. was supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) PGS-D and Ontario Graduate Scholarship; C.E.R. was supported by a Natural Sciences and Engineering Research Council of Canada CGS-D grant; J.F.S. was supported by grants from the National Institutes of Health (HL087216) and the National Science Foundation (OIA-1736249 and IOS-1927675); G.B.M. was supported by a Natural Sciences and Engineering Research Council of Canada Discovery Grant and a Natural Sciences and Engineering Research Council of Canada Discovery Accelerator Supplement; G.R.S. was supported by a Natural Sciences and Engineering Research Council of Canada Discovery Grant and Canada Research Chairs program. Deposited in PMC for release after 12 months.
Publisher Copyright:
© 2020. Published by The Company of Biologists Ltd
PY - 2020
Y1 - 2020
N2 - High-altitude environments are cold and hypoxic, and many high-altitude natives have evolved changes in respiratory physiology that improve O2 uptake in hypoxia as adults. Altricial mammals undergo a dramatic metabolic transition from ectothermy to endothermy in early post-natal life, which may influence the ontogenetic development of respiratory traits at high altitude. We examined the developmental changes in respiratory and haematological traits in deer mice (Peromyscus maniculatus) native to high altitude, comparing the respiratory responses to progressive hypoxia between highland and lowland deer mice. Among adults, highlanders exhibited higher total ventilation and a more effective breathing pattern (relatively deeper tidal volumes), for mice that were caught and tested at their native altitudes and those lab-raised in normoxia. Lab-raised progeny of each population were also tested at post-natal day (P)7, 14, 21 and 30. Highlanders developed an enhanced hypoxic ventilatory response by P21, concurrent with the full maturation of the carotid bodies, and their more effective breathing pattern arose by P14; these ages correspond to critical benchmarks in the full development of homeothermy in highlanders. However, highlanders exhibited developmental delays in ventilatory sensitivity to hypoxia, hyperplasia of type I cells in the carotid body and increases in blood haemoglobin content compared with lowland mice. Nevertheless, highlanders maintained consistently higher arterial O2 saturation in hypoxia across development, in association with increases in blood-O2 affinity that were apparent from birth. We conclude that evolved changes in respiratory physiology in high-altitude deer mice become expressed in association with the post-natal development of endothermy.
AB - High-altitude environments are cold and hypoxic, and many high-altitude natives have evolved changes in respiratory physiology that improve O2 uptake in hypoxia as adults. Altricial mammals undergo a dramatic metabolic transition from ectothermy to endothermy in early post-natal life, which may influence the ontogenetic development of respiratory traits at high altitude. We examined the developmental changes in respiratory and haematological traits in deer mice (Peromyscus maniculatus) native to high altitude, comparing the respiratory responses to progressive hypoxia between highland and lowland deer mice. Among adults, highlanders exhibited higher total ventilation and a more effective breathing pattern (relatively deeper tidal volumes), for mice that were caught and tested at their native altitudes and those lab-raised in normoxia. Lab-raised progeny of each population were also tested at post-natal day (P)7, 14, 21 and 30. Highlanders developed an enhanced hypoxic ventilatory response by P21, concurrent with the full maturation of the carotid bodies, and their more effective breathing pattern arose by P14; these ages correspond to critical benchmarks in the full development of homeothermy in highlanders. However, highlanders exhibited developmental delays in ventilatory sensitivity to hypoxia, hyperplasia of type I cells in the carotid body and increases in blood haemoglobin content compared with lowland mice. Nevertheless, highlanders maintained consistently higher arterial O2 saturation in hypoxia across development, in association with increases in blood-O2 affinity that were apparent from birth. We conclude that evolved changes in respiratory physiology in high-altitude deer mice become expressed in association with the post-natal development of endothermy.
KW - Haemoglobin isoforms
KW - Homeothermy
KW - Hypoxic ventilatory response
KW - Peripheral O chemoreceptor
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U2 - 10.1242/jeb.219360
DO - 10.1242/jeb.219360
M3 - Article
C2 - 32054682
AN - SCOPUS:85081945237
VL - 223
JO - Journal of Experimental Biology
JF - Journal of Experimental Biology
SN - 0022-0949
IS - 4
M1 - jeb219360
ER -