Maternal effect senescence via reduced DNA repair ability in the three‐spined stickleback

Abstract

In many species of animals and plants, survival rate and fertility decrease with advancing age due to senescence. Evolutionary theory explains senescence as a result of age-related declines in the strength of natural selection (Hamilton, 1966), which allow the accumulation of mutations deleterious to late-life performances (Medawar, 1952) and even promote active selection of alleles with deleterious effects in late life but beneficial pleiotropic effects in early life (Williams, 1957). It is well known that advanced maternal age negatively affects not only performance of the mothers, but also health, lifespan and fertility of their offspring in many animal species, including humans ('Lansing effect ': Lansing, 1947;Monaghan et al., 2020). This is mainly due to 'maternal effect senescence',

Effects of maternal age and environmental enrichment on learning ability and brain size

“…The 3-spined stickleback has proven to be an excellent model for investigating the plasticity of the traits directly involved in cognitive processes ( Bell and Foster 1994 ; Brydges et al 2008 ; Feng et al 2015 ). In a parallel experiment, using the same F1 families obtained from the 1-yr-old young females and 2-yr-old senescent females, we demonstrated the presence of maternal effect senescence and showed that the offspring of old mothers had higher rates of malformation and early mortality and had smaller body size at maturity than those of young mothers ( Kim et al 2023 ). In the present experiment, using the offspring obtained from the parallel study, we experimentally tested whether the interplay between maternal age and environmental enrichment experienced during early life affects inhibitory control and learning rate (in a repeated detour-reaching task), brain morphology, growth, survival, and group behavior (i.e.…”

“…Thus, the natural lifespan of this population is less than 18 mo in their native habitat. However, under captive conditions in our laboratory, many fish survive and reproduce until the second breeding season because there is no extrinsic mortality by predation, parasitism, extreme weather, and food limitation ( Kim et al 2023 ).…”

“…The young and old females were in their first and second breeding season, respectively. The breeding design is fully described in a previous study ( Kim et al 2023 ). Briefly, sticklebacks from the 2019 and 2020 cohorts were captured in March 2020 and February 2021, respectively, and kept under laboratory conditions until the 2021 breeding season.…”

“…Gametes from senescent parents are more likely to carry DNA mutations, impaired mitochondrial function, and shorter telomeres ( Gao et al 2019 ; Monaghan and Metcalfe 2019 ; Monaghan et al 2020 ). As mothers experience age-related deterioration, their capacity to transfer maternal resources and substances may also decline, showing maternal effect senescence ( Moorad and Nussey 2016 ; Lemaître and Gaillard 2017 ; Kim et al 2023 ; but see Beamonte-Barrientos et al 2010 ).…”

Directional selection, not the direction of selection, affects telomere length and copy number at ribosomal RNA loci

“…The significant effect of temperature on mtDNA content at 34 °C adds to the diversity of biological impacts that occur in aquatic communities exposed to thermal stress. To our knowledge, only one previous study has examined the effect of temperature on mtDNA content in teleosts, in which there was an increase in mtDNA content in eggs at warmer winter temperatures (+ 5 °C) in stickleback ( Gasterosteus aculeatus ) 97 . Similarly, an increase in mtDNA content was reported in prawns ( Palaemon carinicauda ) raised in warm water 98 .…”