TY - JOUR
T1 - Energetic investment associated with vitellogenesis induces an oxidative cost of reproduction
AU - Webb, Alison C.
AU - Iverson, John B.
AU - Knapp, Charles R.
AU - Denardo, Dale
AU - French, Susannah S.
N1 - Funding Information:
Iguanas were handled, and blood samples were collected and exported with appropriate IACUC (#2530 USU), research permissions (The Bahamas Environment, Science & Technology Commission) and CITES export permits (Bahamas Department of Agriculture). Financial support was provided by Utah State University Research Catalyst Grant project (A35851 to S.S.F.), Utah Agricultural Experiment Station project numbers 1104 and 1347 (S.S.F.), Utah State University Ecology Center (A.C.W.), Shedd Aquarium (C.R.K.), the Earlham College Biology Department (to J.B.I.) and the personal funds of most of the field assistants. Transportation was provided by 7 C's Charters (Bruce Dunham, Sheila Young, Ron White and crew) and the R.V. Coral Reef II (Zoltan Bobick, Kip Mors and Joseph Brozovich). The field assistance of nine Earlham alumni, Bahamas National Trust and BREEF interns, and several Citizen Scientists, Geoff Smith, Jill Jollay and Sandra Buckner, is greatly appreciated. Thank you to our two anonymous reviewers and journal editors for taking the time to provide valuable input on our paper.
Publisher Copyright:
© 2018 The Authors. Journal of Animal Ecology © 2018 British Ecological Society
PY - 2019/3
Y1 - 2019/3
N2 - Oxidative stress is a potential cost of reproduction, but conclusive evidence for this relationship is lacking. The goal of this study was to serially assess across a seasonal gradient the relationship between reproduction, circulating plasma energy metabolites and oxidative state. Here, we examine a study animal ideally suited to test for the oxidative costs of reproduction: the Allen Cays Rock Iguana. Female rock iguanas reproduce at varying frequencies, often skipping years, allowing for a comparison between reproductive and non-reproductive females during the same narrow, annual breeding season. This feature of iguana life history enabled us to address not just sex and seasonal differences in physiology, but also potential oxidative costs of reproduction in females. Male and female iguanas were sampled during the early (vitellogenic), late (gravid) and post-reproductive seasons. Ultrasound examinations were performed on females to quantify reproductive investment, and blood samples were collected for physiology assays, which included reactive oxygen metabolites (d-ROMs), antioxidants, triglycerides, free glycerol and glucose. The early reproductive season was characterized by significant increases in reproductive female's triglycerides, free glycerol and oxidative stress compared to late and post-reproductive periods and non-reproductive females and males during all sampling periods. Antioxidants were significantly elevated during the early reproductive season for reproductive females, non-reproductive females and males when compared to late and post-season. Follicle number in early reproductive females was positively related to d-ROMs, triglycerides and free glycerol, negatively related to antioxidants and showed no relationship with glucose. Measures of oxidative stress, d-ROMs and oxidative index were positively correlated with circulating levels of the lipid metabolite free glycerol during the early reproductive period, but this relationship weakened in the late season and disappeared in the post-season. Broadly, this study supports the hypothesis that the relationship between reproduction and oxidative stress is driven by energy investment, being greatest during early reproduction when vitellogenesis is occurring.
AB - Oxidative stress is a potential cost of reproduction, but conclusive evidence for this relationship is lacking. The goal of this study was to serially assess across a seasonal gradient the relationship between reproduction, circulating plasma energy metabolites and oxidative state. Here, we examine a study animal ideally suited to test for the oxidative costs of reproduction: the Allen Cays Rock Iguana. Female rock iguanas reproduce at varying frequencies, often skipping years, allowing for a comparison between reproductive and non-reproductive females during the same narrow, annual breeding season. This feature of iguana life history enabled us to address not just sex and seasonal differences in physiology, but also potential oxidative costs of reproduction in females. Male and female iguanas were sampled during the early (vitellogenic), late (gravid) and post-reproductive seasons. Ultrasound examinations were performed on females to quantify reproductive investment, and blood samples were collected for physiology assays, which included reactive oxygen metabolites (d-ROMs), antioxidants, triglycerides, free glycerol and glucose. The early reproductive season was characterized by significant increases in reproductive female's triglycerides, free glycerol and oxidative stress compared to late and post-reproductive periods and non-reproductive females and males during all sampling periods. Antioxidants were significantly elevated during the early reproductive season for reproductive females, non-reproductive females and males when compared to late and post-season. Follicle number in early reproductive females was positively related to d-ROMs, triglycerides and free glycerol, negatively related to antioxidants and showed no relationship with glucose. Measures of oxidative stress, d-ROMs and oxidative index were positively correlated with circulating levels of the lipid metabolite free glycerol during the early reproductive period, but this relationship weakened in the late season and disappeared in the post-season. Broadly, this study supports the hypothesis that the relationship between reproduction and oxidative stress is driven by energy investment, being greatest during early reproduction when vitellogenesis is occurring.
KW - antioxidants
KW - free glycerol
KW - reactive oxygen metabolites
KW - reptile
KW - triglycerides
UR - http://www.scopus.com/inward/record.url?scp=85059931469&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85059931469&partnerID=8YFLogxK
U2 - 10.1111/1365-2656.12936
DO - 10.1111/1365-2656.12936
M3 - Article
C2 - 30521087
AN - SCOPUS:85059931469
SN - 0021-8790
VL - 88
SP - 461
EP - 472
JO - Journal of Animal Ecology
JF - Journal of Animal Ecology
IS - 3
ER -