Evidence for reproductive senescence across ray-finned fishes: A review

Abstract

The origin, incidence, and consequences of reproductive senescence vary greatly across the tree of life. In vertebrates, research on reproductive senescence has been mainly focused on mammals and birds, demonstrating that its variation is largely linked to critical life history traits, such as growth patterns, juvenile, and adult mortality, and reproductive strategy. Fishes represent half of the vertebrate taxonomic diversity and display remarkable variation in life history. Based on a thorough literature review, we summarize current evidence on reproductive senescence in ray-finned fishes (Actinopterygii). While survival and physiological senescence are acknowledged in fish, their potential age-related reproductive decline has often been disregarded due to the prevalence of indeterminate growth. We demonstrate that age-related reproductive decline is reported across fish phylogeny, environments, and traits. An important point of our review is that the incidence of reproductive senescence in a species depends on both the number of studies for that species and the coverage of its maximum lifespan by the study. Reproductive senescence was documented for one-third of the studied fish species, with females suffering an age-related decline in reproductive traits less often than males or both parents combined. Neither parental care nor migratory strategy corresponded with the occurrence of reproductive senescence in fish. The traits that were affected by reproductive senescence most often were sex-specific, with pre-mating and mating categories of traits declining in females and sperm quality and quantity in males. We also demonstrate that reproductive senescence can be buffered by indeterminate growth. We provide rich evidence of reproductive senescence across ray-finned fishes, but we highlight the need for better data on age-related reproduction in fishes.

Meta-analysis shows no consistent evidence for senescence in ejaculate traits across animals

“…We suggest several potential non-mutually exclusive reasons for the lack of senescence in our meta-analysis. While we discovered that increasing the proportion of lifespan sampled by a study yielded greater evidence for senescence (also shown by 18 , 35 , 47 ), studies in our meta-analysis tended to sample a low proportion of maximum adult lifespan (median = ~25%, Supplementary Fig. 9 ), which could have underestimated senescence.…”

“…In contrast, some animals show an absence of reproductive senescence 4 . Negligible senescence is predicted in animals with indeterminate growth, like some fish 17 , 18 , where individuals continue to grow post-maturity, thus improving their ability to reproduce throughout their lives due to age-dependent increases in gonad size 8 , 17 . The ability of some animals to maintain cellular repair and sustain homeostasis in reproductive tissues throughout life might also lead to negligible senescence 19 .…”

“…A meta-analytical approach is thus crucial to understand the influence of these ‘moderators’ (Tables 1 and 2 ) and to investigate the general effects of advancing male age on ejaculate traits. Yet, no study has done this systematically for non-human animals (see 35 for humans; 18 for a review in fish; 47 for effects of male age on seminal fluid).…”

Age-dependent decline in sperm quality and function in a naturally short-lived vertebrate

“…For instance, in many insects male reproductive traits, as sperm quality, show an overall negligible age-related decline (4 , but see 15 ), providing support for a constrain in resource allocation. On the contrary, taxa that show continuous growth during life, as fish, are expected to invest more in somatic maintenance than taxa with determinate growth rate ( 16, 17 ). The investment in somatic maintenance is predicted to lead to a greater reproductive senescence and lower actuarial senescence, which is indeed concordant with evidence reported in many fish species ( 16 ).…”

“…On the contrary, taxa that show continuous growth during life, as fish, are expected to invest more in somatic maintenance than taxa with determinate growth rate ( 16, 17 ). The investment in somatic maintenance is predicted to lead to a greater reproductive senescence and lower actuarial senescence, which is indeed concordant with evidence reported in many fish species ( 16 ). However, some fish species, despite showing continuous growth during life, show increased mortality rate with age ( 18 ), raising the question on how trade-offs in resource allocation shape life-history strategy in these species.…”