Fitness correlates of blubber oxidative stress and cellular defences in grey seals (Halichoerus grypus): support for the life-history-oxidative stress theory from an animal model of simultaneous lactation and fasting

被引:2
作者
Armstrong, Holly C. [1 ,2 ]
Russell, Debbie J. F. [3 ]
Moss, Simon E. W. [3 ]
Pomeroy, Paddy [3 ]
Bennett, Kimberley A. [4 ]
机构
[1] Plymouth Univ, Marine Biol & Ecol Res Ctr, Plymouth PL4 8AA, England
[2] Univ St Andrews, Sch Psychol & Neurosci, St Andrews KY16 9JP, Scotland
[3] Univ St Andrews, Scottish Oceans Inst, Sea Mammal Res Unit, St Andrews KY16 8LB, Scotland
[4] Abertay Univ, Sch Appl Sci, Div Hlth Sci, Dundee DD1 1HG, Scotland
基金
英国自然环境研究理事会;
关键词
Cellular stress; Cellular chaperone; Adipose; Trade off; Pinniped; HEAT-SHOCK-PROTEIN; BODY-COMPOSITION; GENE-EXPRESSION; ANTIOXIDANT CAPACITY; CALORIC RESTRICTION; BINDING PROTEIN; REPRODUCTION; OBESITY; COSTS; WILD;
D O I
10.1007/s12192-023-01332-1
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Life-history-oxidative stress theory predicts that elevated energy costs during reproduction reduce allocation to defences and increase cellular stress, with fitness consequences, particularly when resources are limited. As capital breeders, grey seals are a natural system in which to test this theory. We investigated oxidative damage (malondialdehyde (MDA) concentration) and cellular defences (relative mRNA abundance of heat shock proteins (Hsps) and redox enzymes (REs)) in blubber of wild female grey seals during the lactation fast (n = 17) and summer foraging (n = 13). Transcript abundance of Hsc70 increased, and Nox4, a pro-oxidant enzyme, decreased throughout lactation. Foraging females had higher mRNA abundance of some Hsps and lower RE transcript abundance and MDA concentrations, suggesting they experienced lower oxidative stress than lactating mothers, which diverted resources into pup rearing at the expense of blubber tissue damage. Lactation duration and maternal mass loss rate were both positively related to pup weaning mass. Pups whose mothers had higher blubber glutathione-S-transferase (GST) expression at early lactation gained mass more slowly. Higher glutathione peroxidase (GPx) and lower catalase (CAT) were associated with longer lactation but reduced maternal transfer efficiency and lower pup weaning mass. Cellular stress, and the ability to mount effective cellular defences, could proscribe lactation strategy in grey seal mothers and thus affect pup survival probability. These data support the life-history-oxidative stress hypothesis in a capital breeding mammal and suggest lactation is a period of heightened vulnerability to environmental factors that exacerbate cellular stress. Fitness consequences of stress may thus be accentuated during periods of rapid environmental change.
引用
收藏
页码:551 / 566
页数:16
相关论文
共 107 条
[61]   Stress and life history [J].
Monaghan, Pat ;
Spencer, Karen A. .
CURRENT BIOLOGY, 2014, 24 (10) :R408-R412
[62]   Reduced expression of the NADPH oxidase NOX4 is a hallmark of adipocyte differentiation [J].
Mouche, Sarah ;
Ben Mkaddem, Sanae ;
Wang, Wei ;
Katic, Masa ;
Tseng, Yu-Hua ;
Carnesecchi, Stephanie ;
Steger, Klaus ;
Foti, Michelangelo ;
Meier, Christoph A. ;
Muzzin, Patrick ;
Kahn, C. Ronald ;
Ogier-Denis, Eric ;
Szanto, Ildiko .
BIOCHIMICA ET BIOPHYSICA ACTA-MOLECULAR CELL RESEARCH, 2007, 1773 (07) :1015-1027
[63]   Partial pressure of oxygen in adipose tissue and its relationship with fatness in a natural animal model of extreme fat deposition, the grey seal [J].
Oller, Laura ;
Bennett, Kimberley A. ;
McKnight, J. Chris ;
Moss, Simon E. W. ;
Milne, Ryan ;
Hall, Ailsa J. ;
Rocha, Joel .
PHYSIOLOGICAL REPORTS, 2021, 9 (16)
[64]   Molecular and structural antioxidant defenses against oxidative stress in animals [J].
Pamplona, Reinald ;
Costantini, David .
AMERICAN JOURNAL OF PHYSIOLOGY-REGULATORY INTEGRATIVE AND COMPARATIVE PHYSIOLOGY, 2011, 301 (04) :R843-R863
[65]   Oxidative physiology of reproduction in a passerine bird: a field experiment [J].
Pap, Peter L. ;
Vincze, Orsolya ;
Fulop, Attila ;
Szekely-Beres, Orsolya ;
Patras, Laura ;
Penzes, Janka ;
Vagasi, Csongor I. .
BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY, 2018, 72 (02)
[66]   Environments and evolution: interactions between stress, resource inadequacy and energetic efficiency [J].
Parsons, PA .
BIOLOGICAL REVIEWS, 2005, 80 (04) :589-610
[67]   HEAT-SHOCK PROTEINS AND CELL-PROLIFERATION [J].
PECHAN, PM .
FEBS LETTERS, 1991, 280 (01) :1-4
[68]   Measuring Oxidative Stress: The Confounding Effect of Lipid Concentration in Measures of Lipid Peroxidation [J].
Perez-Rodriguez, Lorenzo ;
Romero-Haro, Ana A. ;
Sternalski, Audrey ;
Muriel, Jaime ;
Mougeot, Francois ;
Gil, Diego ;
Alonso-Alvarez, Carlos .
PHYSIOLOGICAL AND BIOCHEMICAL ZOOLOGY, 2015, 88 (03) :345-351
[69]   Note on the unique physiologic state of loggerhead sea turtles (Caretta caretta) during nesting season as evidenced by a suite of health variables [J].
Perrault, Justin R. ;
Stacy, Nicole I. .
MARINE BIOLOGY, 2018, 165 (04)
[70]   Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper - Excel-based tool using pair-wise correlations [J].
Pfaffl, MW ;
Tichopad, A ;
Prgomet, C ;
Neuvians, TP .
BIOTECHNOLOGY LETTERS, 2004, 26 (06) :509-515