The distribution of the Lansing Effect across animal species

Ivimey‐Cook, Edward; Shorr, Sarema; Moorad, Jacob A.

doi:10.1093/evolut/qpac045

Cited by 10 publications

(3 citation statements)

References 47 publications

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“…It is now well known that the age of mothers can affect offspring lifespan and other fitness-related traits in many animal species, including humans, leading to the transmission and accumulation of aging effects in subsequent generations (“Lansing effect”: Lansing 1947 ; Monaghan et al 2020 ; Ivimey-Cook et al 2023 ). Maternal age-related deterioration directly affects offspring’s condition at birth and life-long performance through the declines in genetic integrity of gametes and non-genetic maternal resources and other substances, such as hormones, antibodies, messenger RNA (mRNA) transcripts, and mitochondrial DNA (mtDNA) copies.…”

Section: Introductionmentioning

confidence: 99%

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

Álvarez-Quintero,

Kim

2024

Behavioral Ecology

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It is well known that maternal age at reproduction affects offspring lifespan and some other fitness-related traits, but it remains understudied whether maternal senescence affects how offspring respond to their environments. Early environment often plays a significant role in the development of an animal’s behavioral phenotype. For example, complex environments can promote changes in cognitive ability and brain morphology in young animals. Here, we study whether and how maternal effect senescence influences offspring plasticity in cognition, group behavior, and brain morphology in response to environmental complexity. For this, juvenile 3-spined sticklebacks from young and old mothers (i.e. 1-yr and 2-yr-old) were exposed to different levels of environmental enrichment and complexity (i.e. none, simple, and complex), and their behavior, cognitive ability, and brain size were measured. Exposing fish to enriched conditions improved individual learning ability assessed by a repeated detour-reaching task, increased the size of the whole brain, and decreased aggressive interactions in the shoal. Maternal age did not influence the inhibitory control, learning ability, and group behavioral responses of offspring to the experimental environmental change. However, maternal age affected how some brain regions of offspring changed in response to environmental complexity. In offspring from old mothers, those exposed to the complex environment had larger telencephalons and cerebellums than those who experienced simpler environments. Our results suggest that maternal effect senescence may influence how offspring invest in brain functions related to cognition in response to environmental complexity.

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Section: Introductionmentioning

confidence: 99%

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

Álvarez-Quintero,

Kim

2024

Behavioral Ecology

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“…Reproductive senescence has been relatively well documented in females (Archer et al, 2022;Ivimey-Cook et al, 2023;Nussey et al, 2013;Tarin et al, 2000). Yet, patterns, causes, and consequences of male reproductive senescence are much less understood (Fricke and Koppik, 2019;Kirkwood and Austad, 2000;Lemaitre and Gaillard, 2017).…”

Section: Introductionmentioning

confidence: 99%

No general effects of advancing male age on ejaculates: a meta-analysis across the animal kingdom

Sanghvi

Vega‐Trejo

Nakagawa³

et al. 2023

Preprint

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Senescence, the deterioration of organismal function with advancing age, is a puzzling biological phenomenon. While actuarial senescence (i.e., age-dependent increases in mortality rates) is well described across some taxa, reproductive senescence (i.e.age- dependent declines in reproduction) is less understood, especially in males, with mixed patterns reported across studies. To examine the evidence for male reproductive senescence, we investigated how advancing male age affects ejaculate traits across non-human animals via a meta-analysis yielding 1814 effect sizes from 379 studies. We found no evidence for a general pattern of reproductive senescence. Instead, we found high heterogeneity for how reproduction changes with male age across animals. Some of this heterogeneity (>10%) was associated with biological factors. For example, there were taxonomical differences for some ejaculate traits — sperm motility declined with male age in lab rodents and fish, whereas ejaculate size improved with male age in bulls, fish, and insects. Some methodological factors were also important in explaining this heterogeneity: studies sampling a larger proportion of a species’ lifespan were more likely to detect senescence in ejaculate traits, emphasising the need to examine the full life cycle of species to document senescence. Contrary to predictions, we reveal that the evidence for senescence in ejaculate traits is sporadic. Our findings will help generate novel hypotheses and identify more effective methodological approaches for studying male reproductive senescence.

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“…For instance, offspring sired by old fathers are reported to have poorer development (Janecka et al, 2017;Preston et al, 2015), early-life performance (Fay et al, 2016), and reproductive output (Arslan, 2017;Nystrand and Dowling, 2014;Vuarin et al, 2021), than offspring of young fathers. Notably, offspring born to old fathers often have shorter lifespans than those born to young fathers (Crow, 2003;Monaghan et al, 2020;Sharma et al, 2015), a phenomenon known as the 'Lansing effect' (Ivimey-Cook et al, 2023;Lansing, 1947). While these paternal age effects might be caused by age-dependent changes in paternal care (Benowitz et al, 2013;Cope et al, 2022), in species without care, these effects likely occur via age-dependent deterioration in ejaculates (Monaghan and Metcalfe, 2019).…”

Section: Introductionmentioning

confidence: 99%

What doesn’t kill you makes you stronger? Effects of paternal age at conception on fathers and sons

Sanghvi,

Pizzari,

Sepil

2023

Preprint

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Advancing male age is often hypothesised to reduce both male fertility and offspring quality through reproductive senescence. However, the effects of advancing male age on reproductive output and offspring quality need not always be deleterious. For example, older fathers might compensate for reproductive senescence by terminally investing in reproduction. Similarly, males that survive to reproduce at an old age, might carry alleles that confer high viability (viability selection) which are then inherited by offspring, or might have high reproductive potential (selective disappearance). Differentiating these mechanisms requires an integrated experimental study of paternal survival and reproductive performance, as well as offspring quality, which is currently lacking. UsingDrosophila melanogaster, we test the effects of paternal age at conception (PAC) on paternal survival and reproductive success, and the lifespans of sons. We discover that mating at an old age is temporarily linked with decreased future male survival, suggesting that mating-induced mortality is possibly due to old fathers being frail. We also find a quadratic reproductive ageing pattern, with an onset of senescence in late-life. We discover no evidence for terminal investment, and instead discover positive covariances between a father’s lifespan and his probability of siring offspring, for older PAC groups. Lastly, we show that sons born to older fathers live longer than those born to younger fathers, due to viability selection. Collectively, our results suggest that effects of advancing PAC need not be deleterious for fathers or offspring, and can increase fitness if older fathers produce more viable offspring.Lay summaryIt’s often assumed that old fathers have fewer or lower-quality offspring than young fathers. However, old fathers have on average, usually survived to and reproduced at an older age than young fathers, which might be signals of high quality of old fathers, and benefit offspring. These opposing predictions have rarely been tested, and it’s unclear what their combined influence is, in determining the father’s and offspring’s fitness. Using fruit flies, we explored how old paternal age affects a father’s reproduction and his sons’ lifespans. We find evidence for age-related reproductive decline in fathers. However, we also discover that fathers who mate at an older age live longer than fathers who mate at a younger age, and subsequently, the sons of older fathers live longer than sons of younger fathers. We suggest that the relationship between paternal age, paternal reproduction and lifespan, and offspring quality, is more complex than previously assumed, and that old fathers might provide benefits to their offspring that future studies need to consider.Teaser textIs an old dad really that bad? While old fathers might in some cases produce fewer offspring or offspring of worse quality than young fathers, they have also survived to an older age, thus might be of higher quality. We test how reproducing at an old age affects a father and his son’s fitness. We show that old fathers show evidence of reproductive senescence, but, surprisingly, produce sons that are longer lived than the sons of young fathers. This effect is driven largely by old fathers themselves living longer than young fathers, thus possibly passing alleles conferring higher viability to their sons. Our research is important because it reveals specific mechanisms that drive multifaceted effects of age on fitness.

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The distribution of the Lansing Effect across animal species

Cited by 10 publications

References 47 publications

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

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

No general effects of advancing male age on ejaculates: a meta-analysis across the animal kingdom

What doesn’t kill you makes you stronger? Effects of paternal age at conception on fathers and sons

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