Maternal and Paternal Age Effects on Male Antler Flies: A Field Experiment

Angell, Christopher; Janacek, Rebecca; Rundle, Howard D.

doi:10.1086/718236

Cited by 9 publications

(11 citation statements)

References 42 publications

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“…Whilst the dominant field organism was Homo sapiens ( k = 12, n = 3), the most studied species in the laboratory was Drosophila melanogaster ( k = 28, n = 4). As expected, insect species dominated the laboratory environment ( k = 51/58), and a study of the antler fly ( Protopiophila litigata , Angell et al 2022) provided the sole estimate derived from a natural insect system (Table 1). Strong associations between taxonomy and environments, namely the observation that insects are rarely studied in the field and mammals and birds rarely studied in the laboratory, resemble those reported in a recent review of the relationship between maternal age and early offspring survival (Ivimey-Cook & Moorad, 2020).…”

Section: Resultsmentioning

confidence: 53%

“…2) If the raw data were provided, slopes were estimated by fitting a simple linear model that regressed offspring lifespan against maternal age class. We did this for four studies (Dowling et al 2014, Bouwhuis et al 2015, Lind et al 2015, Angell et al 2022. Where possible, and if the model converged, appropriate random effects (for instance maternal ID) were incorporated to provide a clearer estimate of maternal aging.…”

Section: Methodsmentioning

confidence: 99%

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The distribution of the Lansing Effect across animal species

Ivimey‐Cook

Shorr

Moorad

2022

Preprint

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Maternal senescence is a reduction in individual performance associated with an increase in its mother’s age at conception. When manifested on adult lifespan, this is known as the ‘Lansing Effect’. Single-species studies report both maternal age-related increases and decreases in adult lifespan, but no comprehensive review of the literature has yet determined if the Lansing Effect is a widespread phenomenon. To address this knowledge gap, we performed a meta-analysis of maternal aging rates taken from all available published studies. We recovered 74 estimates from 20 studies representing 14 species. All studies taken together suggest a propensity for a Lansing Effect with an estimated average effect of maternal age on adult lifespan of between -22% to -17% (the lifespan response to an increase in maternal age expressed in the same time units), depending upon our specific choice of model. We failed to find a significant effect of animal class or insect order, but given the oversampling of insect species in the published literature and the paucity of vertebrate studies, we infer that only rotifers and insects demonstrate a tendency for expressing the phenomenon.

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Section: Resultsmentioning

confidence: 53%

Section: Methodsmentioning

confidence: 99%

The distribution of the Lansing Effect across animal species

Ivimey‐Cook

Shorr

Moorad

2022

Preprint

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“…Recently, however, there has been renewed theoretical interest in how offspring quality varies with parental age, especially that of mothers (Gillespie et al 2013;Moorad and Nussey 2016;Barks and Laird 2020;review in Roper et al 2021). Experimental studies testing for paternal age effect on offspring survival and fitness have shown a general decline associated with older fathers, but this pattern is not universal (Monaghan et al 2020;Angell et al 2022). Variation in results among correlational studies could potentially be driven by maternal effects and by other factors confounded with paternal age that are often overlooked (Johnson and Gemmell 2012;Vega-Trejo et al 2018;Cholewa et al 2021;Aich et al 2020b).…”

Section: Discussionmentioning

confidence: 99%

“…Many studies have reported that older fathers produce lower quality offspring (e.g., bulb mite: Prokop et al 2007;mice: García-Palomares et al 2009;cabbage beetles: Liu et al 2011;nerid fly: Wylde et al 2019;bustards: Vuarin et al 2019bustards: Vuarin et al , 2021, partly due to higher offspring mortality rates (e.g., ungulates: Ruiz-López et al 2010;zebra finch: Noguera et al 2018;mice: Xie et al 2018;field crickets: Noguera 2021). On the other hand, some studies have shown that offspring fathered by older males have better early life and adult performance (e.g., fruitflies: Krishna et al 2012;Lee et al 2019;European blackbirds: Cholewa et al 2021), including a higher rate of early life survival (e.g., butterfly: Ducatez et al 2012;zebra fish: Johnson et al 2018;superb fairy-wren: Cooper et al 2020) and longevity (e.g., antler flies: Angell et al 2022). Other studies simply report no detectable effect of paternal age on offspring traits (e.g., ants: Heinze et al 2018;fruitflies: Lee et al 2019;monoandrous moth: Lai et al 2020;common gulls: Sepp et al 2021;burying beetle: Cope et al 2021).…”

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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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“…In general, these studies show that older fathers have a negative effect on offspring lifespan, but the results span the entire outcome space and are sometimes complex (reviewed in [62]). Studies on D. melanogaster [63] and antler flies ( Protopiophila litigata ) [64] found that older fathers in general have longer-lived offspring, while no effect was found in studies of a butterfly [65] and the house sparrow [66]. Negative effects of old fathers have been observed in mice [67,68], the common tern [69] and a neriid fly species [70].…”

Section: Discussionmentioning

confidence: 99%

A genome-wide test for paternal indirect genetic effects on lifespan inDrosophila melanogaster

et al. 2022

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Exposing sires to various environmental manipulations has demonstrated that paternal effects can be non-trivial also in species where male investment in offspring is almost exclusively limited to sperm. Whether paternal effects also have a genetic component (i.e. paternal indirect genetic effects (PIGEs)) in such species is however largely unknown, primarily because of methodological difficulties separating indirect from direct effects of genes. PIGEs may nevertheless be important since they have the capacity to contribute to evolutionary change. Here we use Drosophila genetics to construct a breeding design that allows testing nearly complete haploid genomes (more than 99%) for PIGEs. Using this technique, we estimate the variance in male lifespan due to PIGEs among four populations and compare this to the total paternal genetic variance (the sum of paternal indirect and direct genetic effects). Our results indicate that a substantial part of the total paternal genetic variance results from PIGEs. A screen of 38 haploid genomes, randomly sampled from a single population, suggests that PIGEs also influence variation in lifespan within populations. Collectively, our results demonstrate that PIGEs may constitute an underappreciated source of phenotypic variation.

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Maternal and Paternal Age Effects on Male Antler Flies: A Field Experiment

Cited by 9 publications

References 42 publications

The distribution of the Lansing Effect across animal species

The distribution of the Lansing Effect across animal species

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

A genome-wide test for paternal indirect genetic effects on lifespan inDrosophila melanogaster

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