Lifetime Fitness, Sex-Specific Life History, and the Maintenance of a Polyphenism

Lackey, Alycia C R; Moore, Michael P.; Doyle, Jacqueline; Gerlanc, Nicole; Hagan, Ashley; Geile, Morgan; Eden, C.; Whiteman, Howard H.

doi:10.1086/704156

Cited by 12 publications

(32 citation statements)

References 92 publications

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“…differences in body colour and wing development) or alternative reproductive tactics because morphs or tactics are likely to be affected by different extrinsic factors related to resource acquisition or intrinsic processes causing resource allocation trade‐offs (e.g. Schuett et al., 2015; but see Lackey et al., 2019). For example, in the colour‐dimorphic pea aphid A. pisum , the individual‐level correlation between lifespan and early reproductive investment differs between morphs even when the average values of life‐history traits do not differ between morphs (Schuett et al., 2015).…”

Section: Resultsmentioning

confidence: 99%

Morph‐specific life‐history correlations in a wing‐dimorphic water strider

Hyun

Han

2021

J of Evolutionary Biology

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Life‐history theory predicts a negative correlation between reproduction and survival because individuals differ in their investment in early reproduction at the expense of survival. However, life‐history trade‐offs can be masked when individual differences in resource allocation are smaller than those in resource acquisition. In polymorphic species, as distinct morphs exhibit differences in intrinsic physiology, the relative effects of resource acquisition and allocation on life‐history traits will differ between morphs, contributing to morph‐specific life‐history correlations. Here, in the wing‐dimorphic water strider Aquarius paludum, we found that wing morphs differed in within‐morph individual‐level life‐history correlations. Longer‐lived flight‐capable long‐winged females produced fewer eggs per day and matured later, whereas life‐history trade‐offs were not observed in short‐winged flightless females. The survival–reproduction trade‐off observed in long‐winged females may be a result of individual differences in the timing of wing muscle histolysis. Individuals that underwent wing histolysis early would have increased reproduction at the expense of a shorter life, whereas individuals with late wing histolysis would have reduced reproduction but a longer life. Short‐winged females, who never develop wings, effectively have more resources to allocate to both survival and reproduction, masking any life‐history trade‐offs. Thus, we suggest that morph‐specific effects of resource allocation trade‐offs can shape the morph‐specific extent of individual variation in life‐history strategies, which may contribute to the evolution and maintenance of within‐species polymorphism.

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Section: Resultsmentioning

confidence: 99%

Morph‐specific life‐history correlations in a wing‐dimorphic water strider

Hyun

Han

2021

J of Evolutionary Biology

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“…In palmate newts, considering larger time‐scales, the potential advantages of progenesis in terms of the exploitation of underused resources and earlier reproduction may be counterbalanced by the episodes of drought, favouring metamorphosis, and conditioning the long‐term persistence of progenesis as a polyphenism in these populations (Oromi et al., 2016). Ultimately, only measures of lifetime fitness may allow to decipher between the different factors that may interact in complex ways to influence the success of alternative developmental strategies (Lackey et al., 2019), and identify all the potential costs of progenesis (see also Denoël, Drapeau, Oromi, et al., 2019). Future research on facultative progenesis in this system should aim to address these remaining questions to precise the strength of the ‘trophic advantage of progenesis’ hypothesis along newts lifetime and its role in its success and the long‐term persistence of the polyphenism.…”

Section: Discussionmentioning

confidence: 99%

“…Finally, stable isotope analysis also revealed a lower effect of body size reduction on niche differentiation via progenesis within males than within females. This may constitute a sex‐specific cost of progenesis (Denoël, Drapeau, Winandy, 2019; Lackey et al., 2019; Whiteman, 1997) concurring to explain the low occurrence of progenetic males in palmate newt populations of the Larzac Plateau (Denoël, Drapeau, Winandy, 2019; Mathiron et al., 2017). This effect would add to another disadvantage of progenetic male newts, which are less sexually active than coexisting metamorphic males (Denoël, Drapeau, Winandy, 2019).…”

Section: Discussionmentioning

confidence: 99%

“…However, despite a lower effect of body size reduction on niche differentiation in males than in females, progenesis still clearly gives access to resources that are underused by the ancestral morph for both sexes and could therefore explain their persistence in natural populations. These results along those from lifetime analyses (Lackey et al, 2019) are essential to understand the complex sex-specific payoffs of polyphenisms.…”

Section: Progenesis As An Intrinsic Factor Of Ecological Opportunitymentioning

confidence: 99%

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Progenesis as an intrinsic factor of ecological opportunity in a polyphenic amphibian

et al. 2020

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Paedomorphosis, a developmental heterochrony involving the retention of larval traits at the adult stage, is considered a major evolutionary process because it can generate phenotypic variation without requiring genetic modifications. Two main processes underlie paedomorphosis: neoteny, a slowdown of somatic development, and progenesis, a precocious maturation associated with body size reduction. Being essentially a truncation of ontogeny, progenesis has often been deemed an evolutionary dead end with advantages attributed to precocious reproduction or small body size required in specific environmental contexts (e.g. parasitism, interstitial life), but there is a lack of studies on the immediate ecological consequences of progenesis. Because body size is a key factor determining trophic ecology in animals, we hypothesized that progenesis might intrinsically promote ecological opportunity via body size reduction (i.e. ‘the trophic advantage of progenesis’ hypothesis). We tested this hypothesis in facultatively progenetic palmate newts Lissotriton helveticus using stable isotope niche modelling and diet reconstruction in conjunction with traditional stomach content analyses and body condition (BC) assessment. We show that not only did progenetic individuals occupy a different trophic niche than metamorphic individuals in all populations, but the smaller they were compared to metamorphs due to progenesis, the more different they were in terms of trophic ecology, with no negative effect on their BC. Altogether, the results suggest that via body size reduction, progenesis may generally act as an intrinsic factor of ecological opportunity, allowing the use of existing but previously unavailable resources, even in habitats where seemingly little opportunity exists. We argue that beyond the classically recognized fitness advantages of progenetic development, this process may also generally bring an immediate trophic advantage via body size reduction, which would have important implications to understand the evolution and adaptiveness of this process in many different taxa, from marine meiofauna to primates. A free Plain Language Summary can be found within the Supporting Information of this article.

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“…Numerous studies have developed organizational frameworks for animal life history traits and consequently reveal generalities in life history trade-offs (Pianka, 1970;Pianka et al, 2017;Winemiller et al, 2015), such as the differences between fast strategies (classic r-selected species; early maturity, short lifespans, high reproductive output) and slow strategies (classic K-selected species; late maturity, long lifespans, low reproductive output; Cayuela et al, 2016aCayuela et al, , 2017Healy et al, 2019). Trade-offs in reproductive traits have also been well-documented given the energetic difference for reproduction between males and females (Cayuela et al, 2014(Cayuela et al, , 2016bGrayson et al, 2011;Lackey et al, 2019;Roff & Fairbairn, 1991;Trivers, 1972;Whiteman, 1997). Unsurprisingly, variability and stability of the environment is a primary driver of these life history trade-offs across many animal groups (Cayuela et al, 2017(Cayuela et al, , 2019Mims & Olden, 2012;Pianka, 1970;Townsend & Hildrew, 1994;Winemiller & Rose, 1992).…”

Section: Introductionmentioning

confidence: 99%

The role of environmental variation in mediating fitness trade‐offs for an amphibian polyphenism

Kirk

Reider

Lackey

et al. 2023

Journal of Animal Ecology

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Fitness trade‐offs are a foundation of ecological and evolutionary theory because trade‐offs can explain life history variation, phenotypic plasticity, and the existence of polyphenisms. Using a 32‐year mark‐recapture dataset on lifetime fitness for 1093 adult Arizona tiger salamanders (Ambystoma mavortium nebulosum) from a high elevation, polyphenic population, we evaluated the extent to which two life history morphs (aquatic paedomorphs vs. terrestrial metamorphs) exhibited fitness trade‐offs in breeding and body condition with respect to environmental variation (e.g. climate) and internal state‐based variables (e.g. age). Both morphs displayed a similar response to higher probabilities of breeding during years of high spring precipitation (i.e. not indicative of a morph‐specific fitness trade‐off). There were likely no climate‐induced fitness trade‐offs on breeding state for the two life history morphs because precipitation and water availability are vital to amphibian reproduction. Body condition displayed a contrasting response for the two morphs that was indicative of a climate‐induced fitness trade‐off. While metamorphs exhibited a positive relationship with summer snowpack conditions, paedomorphs were unaffected. Fitness trade‐offs from summer snowpack are likely due to extended hydroperiods in temporary ponds, where metamorphs gain a fitness advantage during the summer growing season by exploiting resources that are unavailable to paeodomorphs. However, paedomorphs appear to have the overwintering fitness advantage because they consistently had higher body condition than metamorphs at the start of the summer growing season. Our results reveal that climate and habitat type (metamorphs as predominately terrestrial, paedomorphs as fully aquatic) interact to confer different advantages for each morph. These results advance our current understanding of fitness trade‐offs in this well‐studied polyphenic amphibian by integrating climate‐based mechanisms. Our conclusions prompt future studies to explore how climatic variation can maintain polyphenisms and promote life history diversity, as well as the implications of climate change for polyphenisms.

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Lifetime Fitness, Sex-Specific Life History, and the Maintenance of a Polyphenism

Cited by 12 publications

References 92 publications

Morph‐specific life‐history correlations in a wing‐dimorphic water strider

Morph‐specific life‐history correlations in a wing‐dimorphic water strider

Progenesis as an intrinsic factor of ecological opportunity in a polyphenic amphibian

The role of environmental variation in mediating fitness trade‐offs for an amphibian polyphenism

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