Reproductive senescence and parental effects in an indeterminate grower

Depeux, Charlotte; Lemaître, Jean‐François; Moreau, Jérôme; Dechaume‐Moncharmont, François‐Xavier; Laverré, Tiffany; Pauhlac, Hélène; Gaillard, Jean‐Michel; Beltran‐Bech, Sophie

doi:10.1111/jeb.13667

Cited by 10 publications

(12 citation statements)

References 64 publications

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“…Paternal age, mating history, and their interaction had no effect on the survival, early-life traits, or immunity of offspring in G. holbrooki. These results are in contrast to other studies that have reported an effect of paternal age on offspring earlylife traits in a wide range of taxa (reviewed in Monaghan et al 2020; also see Cooper et al 2020;Depeux et al 2020;Vuarin et al 2021;Travers et al 2021). However, our results align with an earlier study on G. holbrooki which found no paternal effect, but reported a maternal age effect on offspring early-life traits (Vega-Trejo et al 2018).…”

Section: Discussioncontrasting

confidence: 99%

Separating the effects of paternal age and mating history: Evidence for sex‐specific paternal effect in eastern mosquitofish

2022

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Paternal age and past mating effort by males are often confounded, which can affect our understanding of a father's age effects.To our knowledge, only a few studies have standardized mating history when testing for effects of paternal age, and none has simultaneously disentangled how paternal age and mating history might jointly influence offspring traits. Here, we experimentally manipulated male mating history to tease apart its effects from those of paternal age on female fertility and offspring traits in the eastern mosquitofish (Gambusia holbrooki). Male age did not affect female fertility. However, males with greater past mating effort produced significantly larger broods. Paternal age and mating history interacted to affect sons' body size: sons sired by oldvirgin males were larger than those sired by old-mated males, but this was not the case for younger fathers. Intriguingly, however, sons sired by old-virgin males tended to produce fewer sperms than those sired by old-mated males, indicating a potential tradeoff in beneficial paternal effects. Finally, neither paternal age nor mating history affected daughter's fitness. Our results highlight that variation in offspring traits attributed to paternal age effect could partly arise due to a father's mating history, and not simply to his chronological age.

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Section: Discussioncontrasting

confidence: 99%

Separating the effects of paternal age and mating history: Evidence for sex‐specific paternal effect in eastern mosquitofish

2022

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“…To our knowledge, the only study that carried on ageing and immune priming did not observe similar results: old mealworm beetles did not display an immune priming protection by contrast to young individuals, probably because of immunosenescent process (Daukste et al., 2012). But in our case, A. vulgare lives up to two years, still reproduce until three years old (Al‐Dabbagh & Block, 1981; Depeux et al., 2020; Pitelka & Paris, 1962; Warburg et al., 1984) and live in moist soil, an environment particularly rich in microbial density and diversity (Ranjard & Richaume, 2001; Torsvik et al., 1990), where the risks of infection are high. According to Best et al.…”

Section: Discussionmentioning

confidence: 77%

“…Compared to dipterian models, these crustaceans have a long lifespan (natural populations display 13% of two‐year‐old individuals; Pitelka & Paris, 1962; Warburg et al., 1984), especially suitable for ageing effects’ study (Depeux et al., 2020; Pitelka & Paris, 1962). Age and gender induce variations in their immune parameters (Depeux et al., 2020; Pigeault et al., 2014; Sicard et al., 2010) and several species harbour the maternally transmitted endosymbiont Wolbachia (Bouchon et al., 1998; Cordaux et al., 2012). In the common woodlouse Armadillidium vulgare , this intracellular bacterium feminizes genotypic males into functional phenotypic females (Martin et al., 1973; Rigaud & Juchault, 1993; Bouchon et al, 2008), but also protects the host against some pathogens (Braquart‐Varnier et al., 2015).…”

Section: Introductionmentioning

confidence: 99%

Immune priming depends on age, sex and Wolbachia in the interaction between Armadillidium vulgare and Salmonella

Prigot-Maurice

Araujo

Beltran‐Bech

et al. 2020

J of Evolutionary Biology

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The protection conferred by a first infection upon a second pathogenic exposure (i.e. immune priming) is an emergent research topic in the field of invertebrate immunity. Immune priming has been demonstrated in various species, but little is known about the intrinsic factors that may influence this immune process. In this study, we tested whether age, gender and the symbiotic bacterium Wolbachia affect the protection resulting from immune priming in A. vulgare against S. enterica. We firstly primed young and old, symbiotic and asymbiotic males and females, either with a non‐lethal low dose of S. enterica, LB broth or without injection (control). Seven days post‐injection, we performed a LD50 injection of S. enterica in all individuals and we monitored their survival rates. We demonstrated that survival capacities depend on these three factors: young and old asymbiotic individuals (males and females) expressed immune priming (S. enterica‐primed individuals survived better than LB‐primed and non‐primed), with a general decline in the strength of protection in old females, but not in old males, compared to young. When Wolbachia is present, the immune priming protection was observed in old, but not in young symbiotic individuals, even if the Wolbachia load on entire individuals is equivalent regardless to age. Our overall results showed that the immune priming protection in A. vulgare depends on individuals’ states, highlighting the need to consider these factors both in mechanistical and evolutionary studies focusing on invertebrate's immunity.

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“…Among indeterminately growing invertebrates, common woodlouse (Armadillidium vulgare) females of older ages also produce a higher number of larger offspring. Yet, the offspring of older female woodlouse have lower fitness, offsetting the increase in maternal fertility arising from the indeterminate growth (Depeux et al, 2020). The current datasets indicate that indeterminate growth itself is not sufficient to escape reproductive senescence.…”

Section: Role Of Indeterminate Growth In Fish Reproductive Senescencementioning

confidence: 70%

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

Vrtílek

Žák²,

Reichard³

2022

Front. Ecol. Evol.

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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.

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Reproductive senescence and parental effects in an indeterminate grower

Cited by 10 publications

References 64 publications

Separating the effects of paternal age and mating history: Evidence for sex‐specific paternal effect in eastern mosquitofish

Separating the effects of paternal age and mating history: Evidence for sex‐specific paternal effect in eastern mosquitofish

Immune priming depends on age, sex and Wolbachia in the interaction between Armadillidium vulgare and Salmonella

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

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