The deteriorating soma and the indispensable germline: gamete senescence and offspring fitness

Abstract

The idea that there is an impenetrable barrier that separates the germline and soma has shaped much thinking in evolutionary biology and in many other disciplines. However, recent research has revealed that the so-called ‘Weismann Barrier’ is leaky, and that information is transferred from soma to germline. Moreover, the germline itself is now known to age, and to be influenced by an age-related deterioration of the soma that houses and protects it. This could reduce the likelihood of successful reproduction by old individuals, but also lead to long-term deleterious consequences for any offspring that they do produce (including a shortened lifespan). Here, we review the evidence from a diverse and multidisciplinary literature for senescence in the germline and its consequences; we also examine the underlying mechanisms responsible, emphasizing changes in mutation rate, telomere loss, and impaired mitochondrial function in gametes. We consider the effect on life-history evolution, particularly reproductive scheduling and mate choice. Throughout, we draw attention to unresolved issues, new questions to consider, and areas where more research is needed. We also highlight the need for a more comparative approach that would reveal the diversity of processes that organisms have evolved to slow or halt age-related germline deterioration.

The hidden ageing costs of sperm competition

“…While this transversal study did not reveal any clear difference in the age-specific changes in post-copulatory traits among these three species, it clearly set out a promising framework for future longitudinal studies comparing the age-specific decline in post-copulatory traits over the life course of individuals and across a wider range of species. The study of male reproductive ageing is currently attracting significant attention in evolutionary ecology (Lemaître and Gaillard, 2017;Fricke and Koppik, 2019;Monaghan and Metcalfe, 2019) and such approaches would be particularly relevant to understand the evolutionary roots of male reproductive ageing. 11-IDEX-0007) operated by the French National Research Agency (ANR).…”

Sperm telomere length correlates with blood telomeres and body size in red‐sided garter snakes, Thamnophis sirtalis parietalis

“…Telomere lengths in the blood cells and sperm of individual male redsided garter snakes are correlated, but, on average, sperm telomeres are over 60% longer than blood telomeres, which is similar to the difference between leucocyte and sperm telomeres in humans (Aston et al, 2012). The relationship between ageing and STL is mixed across and within taxa, for example increasing in humans and some mice, but shortening with age in rats and some mice (Aston et al, 2012;de Frutos et al, 2016;Monaghan & Metcalfe, 2019); we find no relationship between STL and age. As we showed in our previous study, blood cell telomeres do not correlate with our proxy for growth; however, in this study, we demonstrate sperm telomere length does correlate with growth, body length and mass.…”

Cross‐Generational Effects of Parental Age on Offspring Longevity: Are Telomeres an Important Underlying Mechanism?

“…Although parental age influences offspring longevity in diverse taxa, the underlying mechanisms are not well understood. Parental age may affect offspring lifespan through many non‐exclusive routes including effects on germline maintenance [ 21–23 ] and age‐related changes in the quality of parental care. [ 24 ] One mechanism that may be particularly important in these contexts is telomeres.…”

“…[ 24 ] One mechanism that may be particularly important in these contexts is telomeres. [ 23,25–28 ] Telomeres are highly conserved, repetitive, sequences of DNA at chromosome ends that enhance genome integrity, but shorten during normal cell division and in response to stress. [ 29 ] Once telomeres become critically short, cells stop dividing and both cell loss and the accumulation of senescent cells are expected to contribute to organismal aging.…”