Physiological Regulation of Growth during Social Ascension in a Group-Living Fish

Abstract

In social groups, dominant animals typically are larger and have better access to resources than subordinates. When subordinates are given the opportunity to ascend to a dominant position, they will elevate their rates of growth to help secure dominance. This study investigated the physiological mechanisms facilitating this increased growth. Using the group-living cichlid, Neolamprologus pulcher, we investigated whether the insulin-like growth factor (IGF) system-a key regulator of growth-is involved in the regulation of growth during social ascension. We also assessed differences in energy storage and expenditure among dominant, subordinate, and ascending males to determine the energetic costs associated with ascension. Daily growth rates tripled during ascension, and ascending males expended more energy after ascension, owing to higher rates of energetically costly social behaviors, increased locomotor activity, and larger home ranges. Ascenders did not increase food intake to offset increasing energetic costs but had half the liver glycogen energy stores of subordinates. Together, these results indicate a reliance on stockpiled energy reserves to fuel the high energetic demands associated with ascension. Transcript abundance of IGF binding proteins 1 (igfbp1) and 2a (igf bp2a) were low in ascenders relative to subordinates, suggesting a higher capacity for growth during ascension through increased bioavailability of circulating IGF-1. Our findings provide clear evidence of the energetic costs of social ascension and offer novel insight into the physiological mechanisms modulating the social regulation of growth.

Sex-dependent growth regulation in monogamous pairs of a cichlid fish

“…Here the feeding rate of J. transcriptus males in female-largest pairs was not related to the initial size ratio of the pairs, and they were unlikely to restrain themselves from feeding according to their relative size within a pair. In some group-living cichlid fishes, subordinates (helpers in cooperative breeding) suppress their body-length growth and instead store resources, leading to BM accumulation (Taborsky, 1984;Heg et al, 2004;Hellmann et al, 2016;Culbert et al, 2019). In our study, body condition deteriorated in approximately 30% of J. transcriptus males over time in female-largest pairs, and such deterioration was more conspicuous in pairs with a small initial size ratio.…”

Emergence of size-structured dominance hierarchies through size-dependent feedback

“…In the goby P. xanthosomas subordinates refrain from eating when size differences are small [44]. Changes in growth rate are associated with changes in allocation of energy to reserves versus growth in N. pulcher [47]. Finally, social interactions, including submissive behaviour, are often energetically costly [55], and the frequency of submissive displays increases at smaller size differences [43], so changes in energy expenditure may contribute to growth suppression.…”

“…However, growth can be influenced by social context in other ways. In N. pulcher , newly ascended dominants grow rapidly [ 4 , 21 , 47 ]. This pattern is also observed in several highly social mammals [ 56 – 59 ] and in the cichlid, Astatotilapia burtoni [ 60 ] in which loss of rank is also associated with reduced growth.…”

“…Size-based conflict between individuals i and j influences j's growth by reducing the anabolic constant ( A ) by some proportion U ji . We do not specify the mechanism underlying growth suppression; growth regulation could result through self-restraint [ 44 ], shifts in energy allocation [ 47 ] or by individuals directly preventing growth of their partners in some way (e.g. excluding them from resources when similar in size [ 26 ]).…”

Social rank influences relationships between hormones and oxidative stress in a cichlid fish

“…We targeted the gonads because dominant males have larger gonads than subordinate males (Huffman et al, 2012; Maruska and Fernald, 2011) and because they are the primary site for the synthesis of testosterone (Payne and Hales, 2004; Tokarz et al, 2015). As well, we targeted the liver because energetic/metabolic processes in the liver often vary with social rank (Culbert et al, 2019; Gilmour et al, 2012; Kostyniuk et al, 2018) and the liver is one of the primary targets for the metabolic actions of cortisol (Culbert et al, 2021; Faught and Vijayan, 2016; Mommsen et al, 1999).…”