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An eco-evolutionary feedback loop between population dynamics and fighter expression affects the evolution of alternative reproductive tactics.

ABSTRACT: Surprisingly, little is known about how eco-evolutionary feedback loops affect trait dynamics within a single population. Polymorphisms of discrete alternative phenotypes present ideal test beds to investigate this, as the alternative phenotypes typically exhibit contrasting demographic rates mediated through frequency or density dependence, and are thus differentially affected by selection. Alternative reproductive tactics (ARTs), like male fighters and sneakers, are an extreme form of discrete phenotype expression and occur across many taxa. Fighters possess weapons for male-male competition over access to mates, whereas sneakers are defenceless but adopt tactics like female-mimicking. Because fighters in some species mortally injure conspecifics, this raises the question whether fighter expression can feed back to affect population size and structure, thereby altering the selection gradient and evolutionary dynamics of ART expression in an eco-evolutionary feedback loop. Here, we investigated how the eco-evolutionary feedback loop between fighter expression and population size and structure affects the evolution and maintenance of ARTs. We introduced intraspecific killing by fighters in a two-sex, two-ART population model parameterized for the male dimorphic bulb mite (Rhizoglyphus robini) that includes life-history differences between the ARTs and a mating-probability matrix analogous to the classic hawk-dove game. Using adaptive dynamics, we found that the intraspecific killing by fighters can extend the range of life-history parameter values under which ARTs evolve, because fighters that kill other fighters decrease fighter fitness. This effect can be nullified when benefits from killing are incorporated, like increased reproduction through increased energy uptake. The eco-evolutionary feedback effects found here for a dimorphic trait likely also occur in other fitness-related traits, such as behavioural syndromes, parental care and niche construction traits. Current theoretical advances to model eco-evolutionary processes, and empirical steps towards unravelling the underlying drivers, pave the way for understanding how selection affects trait evolution in an eco-evolutionary feedback loop.

SUBMITTER: Croll JC

PROVIDER: S-EPMC7380021 | biostudies-literature | 2019 Jan

REPOSITORIES: biostudies-literature

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An eco-evolutionary feedback loop between population dynamics and fighter expression affects the evolution of alternative reproductive tactics.

Croll Jasper C JC Egas Martijn M Smallegange Isabel M IM

The Journal of animal ecology 20180919 1

Surprisingly, little is known about how eco-evolutionary feedback loops affect trait dynamics within a single population. Polymorphisms of discrete alternative phenotypes present ideal test beds to investigate this, as the alternative phenotypes typically exhibit contrasting demographic rates mediated through frequency or density dependence, and are thus differentially affected by selection. Alternative reproductive tactics (ARTs), like male fighters and sneakers, are an extreme form of discrete ...[more]

PMID: 30125360

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Project description:Alternative reproductive tactics (ARTs), discrete phenotypic variations evolved to maximize fitness, may entail different cost-benefit trade-offs. In large mammals, differences in costs associated with ARTs-including energy expenditure and parasite infection-are typically greatest during the breeding season. Nonetheless, physiological and behavioral differences between ARTs can manifest throughout the year, possibly involving costs that may contribute to maintain ARTs within populations. Using the number of nematode larvae per gram of feces (LPG) as a proxy, we explored the temporal changes in lung parasite infection in territorial and nonterritorial male chamois Rupicapra in the Gran Paradiso National Park (Italy), between 2011 and 2012. We aimed to identify which tactic-specific physiological and behavioral features (including age, hormonal levels, inter- and intrasexual interactions, and space use) or climatic factors (temperature and precipitation) best explained yearly variation in parasite infection within and between ARTs. Generalized additive mixed models showed that the fecal larval counts of lung nematodes underwent strong temporal changes in both male types. Differences between ARTs (with higher LPG values in territorial than nonterritorial males) were greatest during the rut and-to a lesser extent-in spring, respectively, at the peak and at the onset of territoriality. The difference in LPG between tactics was largely explained by the greater levels of hormone metabolites in territorial males during the rut. The other variables did not contribute significantly to explain the different shedding of larvae within and between ARTs. Our analysis suggests that different values of LPG between territorial and nonterritorial males are largely a result of tactic-specific differences in the secretion of hormone metabolites, but only during the rut. To clarify whether rut-related parasitism contributes to the maintenance of ARTs, tactic-specific life history trade-offs, for example, between reproduction and parasite-related mortality, must be investigated.

Project description:BackgroundAlternative reproductive tactics (ARTs) are taxonomically pervasive strategies adopted by individuals to maximize reproductive success within populations. Even for conditionally-dependent traits, consensus postulates most ARTs involve both genetic and environmental interactions (GEIs), but to date, quantifying genetic variation underlying the threshold disposing an individual to switch phenotypes in response to an environmental cue has been a difficult undertaking. Our study aims to investigate the origins and maintenance of ARTs within environmentally disparate populations of the microscopic bulb mite, Rhizoglyphus robini, that express 'fighter' and 'scrambler' male morphs mediated by a complex combination of environmental and genetic factors.ResultsUsing never-before-published individual genetic profiling, we found all individuals across populations are highly inbred with the exception of scrambler males in stressed environments. In fact within the poor environment, scrambler males and females showed no significant difference in genetic differentiation (Fst) compared to all other comparisons, and although fighters were highly divergent from the rest of the population in both poor or rich environments (e.g., Fst, STRUCTURE), fighters demonstrated approximately three times less genetic divergence from the population in poor environments. AMOVA analyses further corroborated significant genetic differentiation across subpopulations, between morphs and sexes, and among subpopulations within each environment.ConclusionOur study provides new insights into the origin of ARTs in the bulb mite, highlighting the importance of GEIs: genetic correlations, epistatic interactions, and sex-specific inbreeding depression across environmental stressors. Asymmetric reproductive output, coupled with the purging of highly inbred individuals during environmental oscillations, also facilitates genetic variation within populations, despite evidence for strong directional selection. This cryptic genetic variation also conceivably facilitates stable population persistence even in the face of spatially or temporally unstable environmental challenges. Ultimately, understanding the genetic context that maintains thresholds, even for conditionally-dependent ARTs, will enhance our understanding of within population variation and our ability to predict responses to selection.

Project description:Life history theory predicts that the amount of resources allocated to reproduction should maximize an individual's lifetime reproductive success. So far, resource allocation in reproduction has been studied mainly in females. Intraspecific variation of endogenous energy storage and utilization patterns of males has received little attention, although these patterns may vary greatly between individuals pursuing alternative reproductive tactics (ARTs). ARTs are characterized by systematic variation of behavioral, physiological, and often morphological traits among same-sex conspecifics. Some individuals may rely on previously accumulated reserves, because of limited foraging opportunities during reproduction. Others may be able to continue foraging during reproduction, thus relying on reserves to a lesser extent. We therefore predicted that, if male tactics involve such divergent limitations and trade-offs within a species, ARTs should correspondingly differ in energy reserve allocation and utilization. To test this prediction, we studied short-term and long-term reserve storage patterns of males in the shell-brooding cichlid Lamprologus callipterus. In this species, bourgeois males investing in territory defense, courtship, and guarding of broods coexist with two distinct parasitic male tactics: (1) opportunistic sneaker males attempting to fertilize eggs by releasing sperm into the shell opening when a female is spawning; and (2) specialized dwarf males attempting to enter the shell past the spawning female to fertilize eggs from inside the shell. Sneaker males differed from other male types by showing the highest amount of accumulated short-term and long-term fat stores, apparently anticipating their upcoming adoption of the nest male status. In contrast, nest males depleted previously accumulated energy reserves with increasing nest holding period, as they invest heavily into costly reproductive behaviors while not taking up any food. This conforms to a capital breeder strategy. Dwarf males did not accumulate long-term fat stores at all, which they can afford due to their small behavioral effort during reproduction and their continued feeding activity, conforming to an income breeder strategy. Our data confirm that the resource storage patterns of males pursuing ARTs can diverge substantially, which adds to our understanding of the coexistence and maintenance of alternative reproductive patterns within species.

Dataset Information

An eco-evolutionary feedback loop between population dynamics and fighter expression affects the evolution of alternative reproductive tactics.

Publications

An eco-evolutionary feedback loop between population dynamics and fighter expression affects the evolution of alternative reproductive tactics.

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