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Oxidative costs of cooperation in cooperatively breeding Damaraland mole-rats.

ABSTRACT: Within cooperatively breeding societies, individuals adjust cooperative contributions to maximize indirect fitness and minimize direct fitness costs. Yet, little is known about the physiological costs of cooperation, which may be detrimental to direct fitness. Oxidative stress, the imbalance between reactive oxygen species (by-products of energy production) and antioxidant protection, may represent such a cost when cooperative behaviours are energetically demanding. Oxidative stress can lead to the accumulation of cellular damage, compromising survival and reproduction, thus mediating the trade-off between these competing life-history traits. Here, we experimentally increased energetically demanding cooperative contributions in captive Damaraland mole-rats (Fukomys damarensis). We quantified oxidative stress-related effects of increased cooperation on somatic and germline tissues, and the trade-off between them. Increased cooperative contributions induced oxidative stress in females and males, without increasing somatic damage. Males accumulated oxidative damage in their germline despite an increase in antioxidant defences. Finally, oxidative damage accumulation became biased towards the germline, while antioxidant protection remained biased towards the soma, suggesting that males favour the maintenance of somatic tissues (i.e. survival over reproduction). Our results show that heightened cooperative contributions can ultimately affect direct fitness through oxidative stress costs, which may represent a key selective pressure for the evolution of cooperation.

SUBMITTER: Mendonca R

PROVIDER: S-EPMC7542782 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:IntroductionThe Damaraland mole-rat (Fukomys damarensis) is a eusocial, subterranean mammal, which exhibits an extreme reproductive skew with a single female (queen) monopolizing reproduction in each colony. Non-reproductive females in the presence of the queen are physiologically suppressed to the extent that they are anovulatory. This blockade is thought to be caused by a disruption in the normal gonadotropin-releasing hormone (GnRH) secretion from the hypothalamus. In order to understand the underlying physiological mechanisms of reproductive suppression in subordinate females we studied the expression of steroid hormone receptors and the androgen-converting enzyme aromatase in forebrain regions involved in the control of reproductive behaviour in female breeders and non-breeders from intact colonies. Additionally, we included in our analysis females that experienced the release from social suppression by being removed from the presence of the queen.ResultsWe found expression of androgen receptor, estrogen receptor α and aromatase in several forebrain regions of female Damaraland mole-rats. Their distribution matches previous findings in other mammals. Quantification of the hybridisation signal revealed that queens had increased expression of androgen receptors compared to non-breeders and removed non-breeders in most brain regions examined, which include the medial preoptic area (MPOA), the principal nucleus of the bed nucleus of the stria terminalis (BSTp), the ventromedial nucleus of the hypothalamus (VMH), the arcuate nucleus (ARC) and the medial amygdala (MeA). Furthermore, breeders had increased estrogen receptor α expression in the anteroventral periventricular nucleus (AVPV) and in the MeA, while aromatase expression in the AVPV was significantly reduced compared to non-breeders. Absence of social suppression was associated with increased androgen receptor expression in the ARC, increased estrogen receptor α expression in the MeA and BSTp and reduced aromatase expression in the AVPV.ConclusionThis study shows that social suppression and breeding differentially affect the neuroendocrine phenotype of female Damaraland mole-rats. The differential expression pattern of estrogen receptor α and aromatase in the AVPV between breeders and non-breeders supports the view that this region plays an important role in mediating the physiological suppression in subordinate females.

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Oxidative costs of cooperation in cooperatively breeding Damaraland mole-rats.

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