Adiponectin and Insulin in Gray Seals during Suckling and Fasting: Relationship with Nutritional State and Body Mass during Nursing in Mothers and PupsPhysiological and Biochemical Zoology

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Authors
K. A. Bennett, J. Hughes, S. Stamatas, S. Brand, N. L. Foster, S. E. W. Moss, P. P. Pomeroy
Year
2015
DOI
10.1086/680862
Subject
Physiology / Animal Science and Zoology / Biochemistry

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Text

Adiponectin and Insulin in Gray Seals during Suckling and Fasting:

Relationship with Nutritional State and Body Mass during

Nursing in Mothers and Pups

K. A. Bennett1,*

J. Hughes1

S. Stamatas1

S. Brand1

N. L. Foster1

S. E. W. Moss2

P. P. Pomeroy2 1Marine Biology and Ecology Research Centre, School of

Marine Science and Engineering, Plymouth University,

Portland Square, Drake Circus, Plymouth, Devon PL4 8AA,

United Kingdom; 2Natural Environment Research Council

Sea Mammal Research Unit, Gatty Marine Laboratories,

Scottish Oceans Institute, University of St. Andrews,

St. Andrews, Fife KY16 8LB, United Kingdom

Accepted 1/27/2015; Electronically Published 3/4/2015

ABSTRACT

Animals that fast during breeding and/or development, such as phocids, must regulate energy balance carefully to maximize reproductive fitness and survival probability. Adiponectin, produced by adipose tissue, contributes to metabolic regulation by modulating sensitivity to insulin, increasing fatty acid oxidation by liver and muscle, and promoting adipogenesis and lipid storage in fat tissue. We tested the hypotheses that (1) circulating adiponectin, insulin, or relative adiponectin gene expression is related to nutritional state, body mass, and mass gain in wild gray seal pups; (2) plasma adiponectin or insulin is related to maternal lactation duration, body mass, percentage milk fat, or free fatty acid (FFA) concentration; and (3) plasma adiponectin and insulin are correlated with circulating FFA in females and pups. In pups, plasma adiponectin decreased during suckling (linear mixed-effects model [LME]: Tp 4.49;

P ! 0.001) and the early postweaning fast (LME: Tp 3.39; Pp 0.004). In contrast, their blubber adiponectin gene expression was higher during the early postweaning fast than early in suckling (LME: Tp 2.11; Pp 0.046). Insulin levels were significantly higher in early (LME: Tp 3.52; Pp 0.004) and late (LME: Tp 6.99; P ! 0.001) suckling than in fasting and, given the effect of nutritional state,were also positively related to body mass (LME: T p 3.58; P p 0.004). Adiponectin and insulin levels did not change during lactation and were unrelated to milk FFA or percentage milk fat in adult females. Our data suggest that adiponectin, in conjunction with insulin, may facilitate fat storage in seals and is likely to be particularly important in the development of blubber reserves in pups.

Introduction

The allocation of energy by female capital breeders and their offspring during nursing is important in understanding lifehistory decisions and lactation strategies (Boggs 1992; Oftedal et al. 1993; Boyd 2000; Crocker et al. 2001). Energy allocation links foraging and reproductive success and, thus, ultimately indicates how individuals and populations may respond to variation in food availability (Boggs 1992; Jönsson 1997; Boyd 2000; Crocker et al. 2001). Capital breeders store energy in advance of reproduction and then utilize those body energy stores to attempt to breed successfully (Jönsson 1997). Careful management of their energy balance is thus central to maximizing their reproductive fitness and survival potential (Calow 1979). Femalesmust possess sufficient energy to “finance” their reproductive expenditure and must allocate reserves judiciously to both sustain their own metabolism and invest in the young at least enough to nurse them to independence (Jönsson 1997). The young must also be able to maximize energy provided by the mother in terms of rapid growth or fat storage (Oftedal et al. 1993; Lindström 1999; Hou et al. 2008).

Fuel allocationmust be based, at least in part, on information derived from the availability of metabolic fuel. Endogenous signals that link energy stores with fuel use are well documented in many terrestrial mammals and birds (Woods and Seeley 2000; Benoit et al. 2004). They incorporate a variety of inputs, including circulating levels of metabolites and/or hormones involved in energy balance. Adipose tissue itself is a large endocrine organ and an important regulator of body energy reserves (Trayhurn and Beattie 2001; Kershaw and Flier 2004). It produces an array of physiologically important fat-regulating hormones, termed adipocytokines, which can act centrally to influence appetite andmetabolic rate and locally to regulate the balance between lipolysis and lipogenesis (Ahima and Flier 2000; Meier and Gressner 2004; Qi et al. 2004). *Corresponding author; e-mail: kimberley.bennett@plymouth.ac.uk.

Physiological and Biochemical Zoology 88(3):295–310. 2015. q 2015 by The

University of Chicago. All rights reserved. 1522-2152/2015/8803-4122$15.00.

DOI: 10.1086/680862 295

Adiponectin (ACRP30, ApN, or ADIPOQ) is an adipocytokine with key roles in energy balance, acting primarily through powerful insulin-sensitizing effects at the wholeanimal and cellular levels (Hu et al. 1996; Berg et al. 2001, 2002; Hotta et al. 2001; Gao et al. 2013). Adiponectin levels and adiponectin messenger RNA (mRNA) abundance negatively correlate with indices of body fat content and insulin sensitivity in dogs, pigs, cows, and primates (Arita et al. 1999;

Hotta et al. 2001; Jacobi et al 2004; Ishioka et al. 2006;

Taniguchi et al. 2008; Cahill et al. 2013; Gao et al. 2013).

Adiponectin mRNA is found exclusively in adipocytes, and its expression is increased up to ~400-fold during their differentiation (Scherer et al. 1995; Körner et al. 2005). In contrast to its effects on muscle and liver, in which it stimulates fatty acid clearance and fatty acid oxidation (Fruebis et al. 2001;

Yamauchi et al. 2001; Berg et al. 2002; Thamer et al. 2002;

Tomas et al. 2002; Combs et al. 2004), in fat tissue, adiponectin accelerates lipid accumulation during adipogenesis, promoting both proliferation and differentiation of preadipocytes (Fu et al. 2005). Adiponectin has no effect on lipolysis and appears to suppress de novo fatty acid synthesis in adipocytes (Jacobi et al. 2004). However, it enhances insulinresponsive glucose transport and fatty acid uptake and promotes their esterification into triglyceride for fat storage (Combs et al. 2004). Mice with a deletion in the adiponectin gene that causes them to have threefold higher plasma concentrations of the hormone have 30% body fat, compared with only 18% in wild-type littermates (Combs et al. 2004). Adiponectin is thus a powerful driver of adipocyte maturation, triglyceride synthesis, and storage in fat cells. Given the importance of adiponectin in fuel regulation in other species, adiponectin may be a key endocrine signal in energy balance regulation in capital breeders.