Understanding Reproductive Aging in Wildlife to Improve Animal Conservation and Human Reproductive Health

Abstract

Similar to humans and laboratory animals, reproductive aging is observed in wild species-from small invertebrates to large mammals. Aging issues are also prevalent in rare and endangered species under human care as their life expectancy is longer than in the wild. The objectives of this review are to (1) present conserved as well as distinctive traits of reproductive aging in different wild animal species (2) highlight the value of comparative studies to address aging issues in conservation breeding as well as in human reproductive medicine, and (3) suggest next steps forward in that research area. From social insects to mega-vertebrates, reproductive aging studies as well as observations in the wild or in breeding centers often remain at the physiological or organismal scale (senescence) rather than at the germ cell level. Overall, multiple traits are conserved across very different species (depletion of the ovarian reserve or no decline in testicular functions), but unique features also exist (endless reproductive life or unaltered quality of germ cells). There is a broad consensus about the need to fill research gaps because many cellular and molecular processes during reproductive aging remain undescribed. More research in male aging is particularly needed across all species. Furthermore, studies on reproductive aging of target species in their natural habitat (sentinel species) are crucial to define more accurate reproductive indicators relevant to other species, including humans, sharing the same environment. Wild species can significantly contribute to our general knowledge of a crucial phenomenon and provide new approaches to extend the reproductive lifespan.

Timeless or tainted? The effects of male ageing on seminal fluid

“…Onset and rate of age-related biological decline and impaired reproductive function varies between males and females (Bronikowski et al, 2022). There has been a long-standing focus on females in lifehistory research, and studies have only recently begun to consider male reproductive ageing (e.g., Fricke and Koppik, 2019;Comizzoli and Ottinger, 2021;Archer et al, 2022). Evidence suggests that male reproductive ageing can affect male fertilizing ability (Paul and Robaire, 2013;Aich et al, 2021), influence female behavior (Dean et al, 2010;Vuarin et al, 2019), and lead to paternal effects on offspring (Daxinger and Whitelaw, 2012).…”

Sex‐specific aging in animals: Perspective and future directions

“…At the population scale, such deterioration in organismal phenotypes often manifests as declining fertility and increasing mortality with advancing adult age. It is well known that animal reproductive aging can differ between the sexes (reviewed in Comizzoli & Ottinger, 2021 ), with an extreme example being reproductive cessation in some female, but not male mammals (Alberts et al, 2013 ) with a long post‐reproductive lifespan being seen in human females (Levitis et al, 2013 ). Remarkably, sex differences in lifespan are observed in many animal species as well and can encompass differences between males and females in the age‐of‐onset of senescence, the rate of increase in age‐specific mortality, and/or the initial mortality rate in early adulthood—all of which can lead to sex‐specific aging trajectories.…”

“…Other aspects of senescence also show sex differences in diverse animal taxa. For example, reproductive potential declines with age at different rates in males and females of many species (Comizzoli & Ottinger, 2021 ; Holmes et al, 2001 ). In the red wolf, Canis rufus , male reproductive success, as measured by pup recruitment, declines with age, while no such decline is observed in females (Sparkman et al, 2017 ).…”

Reproductive Senescence in Two Lemur Lineages

“…If the detrimental age-effects cannot be fully compensated by reduced reproductive rates, infant survival may also be compromised. Even if females continue to reproduce at regular intervals throughout their lifetime, advanced maternal age may result in increased rates of miscarriages or negatively affect offspring survival because of reduced birth weights, milk production or other complications (Atsalis and Margulis, 2008;Lemaître and Gaillard, 2017;Comizzoli and Ottinger, 2021). In fact, infant survival in female olive baboons rapidly declined with age, and mothers beyond 21 years of age were more likely to experience a miscarriage (Packer et al, 1998).…”