Abstract
BackgroundNaked mole-rats (NMRs) are eusocially organized in colonies. Although breeders carry the additional metabolic load of reproduction, they are extremely long-lived and remain fertile throughout their lifespan. This phenomenon contrasts the disposable soma theory of aging stating that organisms can invest their resources either in somatic maintenance, enabling a longer lifespan, or in reproduction, at the cost of longevity. Here, we present a comparative transcriptome analysis of breeders vs. non-breeders of the eusocial, long-lived NMR vs. the polygynous and shorter-lived guinea pig (GP).ResultsComparative transcriptome analysis of tissue samples from ten organs showed, in contrast to GPs, low levels of differentiation between sexes in adult NMR non-breeders. After transition into breeders, NMR transcriptomes are markedly sex-specific, show pronounced feedback signaling via gonadal steroids, and have similarities to reproductive phenotypes in African cichlid fish, which also exhibit social status changes between dominant and subordinate phenotypes. Further, NMRs show functional enrichment of status-related expression differences associated with aging. Lipid metabolism and oxidative phosphorylation—molecular networks known to be linked to aging—were identified among most affected gene sets. Remarkably and in contrast to GPs, transcriptome patterns associated with longevity are reinforced in NMR breeders.ConclusionOur results provide comprehensive and unbiased molecular insights into interspecies differences between NMRs and GPs, both in sexual maturation and in the impact of reproduction on longevity. We present molecular evidence that sexual maturation in NMRs is socially suppressed. In agreement with evolutionary theories of aging in eusocial organisms, we have identified transcriptome patterns in NMR breeders that—in contrast to the disposable soma theory of aging—may slow down aging rates and potentially contribute to their exceptional long life- and healthspan.
Highlights
Naked mole-rats (NMRs) are eusocially organized in colonies
We focused our analyses on transcriptome signatures of the sexually dormant NMR non-breeders and the differentially expressed genes (DEGs) that may contribute to the exceptional long life- and healthspan of NMR breeders
To gain molecular insights into the fascinating combination of NMR phenotypes, in particular, their eusocial reproduction, lifelong fertility, extraordinary healthspan, and longevity, we aimed to collect a comprehensive set of tissues for male and female breeders and non-breeders of NMR and guinea pig (GP)—six biological replicates each
Summary
Breeders carry the additional metabolic load of reproduction, they are extremely long-lived and remain fertile throughout their lifespan This phenomenon contrasts the disposable soma theory of aging stating that organisms can invest their resources either in somatic maintenance, enabling a longer lifespan, or in reproduction, at the cost of longevity. The unique biology of the naked mole-rat (NMR, Heterocephalus glaber) has fostered its increasing popularity as an animal model in a variety of research fields This includes an exceptionally long lifespan and resistance to cancer [1, 2]. It was shown that closely related African Fukomys mole-rats, which have a eusocial structure similar to NMRs, show lifespan differences between reproductive and non-reproductive animals [18, 19] Those observations contrast the disposable soma theory of aging. In the case of low-extrinsic mortality, it seems to be more effective to allocate resources to somatic tissue, thereby keeping the body healthy and enabling a longer reproduction during a longer lifespan
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