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Is diversification in male reproductive traits driven by evolutionary trade-offs between weapons and nuptial gifts?

ABSTRACT: Many male animals have evolved exaggerated traits that they use in combat with rival males to gain access to females and secure their reproductive success. But some male animals invest in nuptial gifts that gains them access to females. Both these reproductive strategies are costly in that resources are needed to produce the weapon or nuptial gift. In closely related species where both weapons and nuptial gifts are present, little is known about the potential evolutionary trade-off faced by males that have these traits. In this study, we use dobsonflies (order Megaloptera, family Corydalidae, subfamily Corydalinae) to examine the presence and absence of enlarged male weapons versus nuptial gifts within and among species. Many dobsonfly species are sexually dimorphic, and males possess extremely enlarged mandibles that they use in battles, whereas in other species, males produce large nuptial gifts that increase female fecundity. In our study, we show that male accessory gland size strongly correlates with nuptial gift size and that when male weapons are large, nuptial gifts are small and vice versa. We mapped weapons and nuptial gifts onto a phylogeny we constructed of 57 species of dobsonflies. Our among-species comparison shows that large nuptial gift production evolved in many species of dobsonfly but is absent from those with exaggerated weapons. This pattern supports the potential explanation that the trade-off in resource allocation between weapons and nuptial gifts is important in driving the diversity of male mating strategies seen in the dobsonflies, whereas reduced male-male competition in the species producing large spermatophores could be an alternative explanation on their loss of male weapons. Our results shed new light on the evolutionary interplay of multiple sexually selected traits in animals.

SUBMITTER: Liu X

PROVIDER: S-EPMC4424648 | biostudies-literature | 2015 May

REPOSITORIES: biostudies-literature

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Is diversification in male reproductive traits driven by evolutionary trade-offs between weapons and nuptial gifts?

Liu Xingyue X Hayashi Fumio F Lavine Laura C LC Yang Ding D

Proceedings. Biological sciences 20150501 1807

Many male animals have evolved exaggerated traits that they use in combat with rival males to gain access to females and secure their reproductive success. But some male animals invest in nuptial gifts that gains them access to females. Both these reproductive strategies are costly in that resources are needed to produce the weapon or nuptial gift. In closely related species where both weapons and nuptial gifts are present, little is known about the potential evolutionary trade-off faced by male ...[more]

PMID: 25925103

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Project description:BackgroundMany male animals donate nutritive materials during courtship or mating to their female mates. Donation of large-sized gifts, though costly to prepare, can result in increased sperm transfer during mating and delayed remating of the females, resulting in higher paternity. Nuptial gifting sometimes causes severe female-female competition for obtaining gifts (i.e., sex-role reversal in mate competition) and selection on females to increase their mating rate, changing the intensity of sperm competition and the resultant paternity gains. We built a theoretical model to simulate such coevolutionary feedbacks between nuptial gift size (male trait) and propensity for multiple mating (female trait). Donation of nuptial gifts sometimes causes development of female persistence trait for gift acquisition. We also analyzed the causes and consequences of this type of traits, taking double receptacles for nutritious seminal gifts, which are known to occur in an insect group with a "female penis" (Neotrogla spp.), as an illustrative example.ResultsOur individual-based simulations demonstrated that female-female competition for male-derived nutrients always occur when the environment is oligotrophic and mating costs are low for females. However, a positive correlation between donated gift size and the resultant paternity gain was a requisite for the co-occurrence of large gifts and females' competitive multiple mating for the gifts. When gift donation satisfied female demands and thus resulted in monandry, exaggeration of nuptial gift size also occurred under the assumption that the last male monopolizes paternity. The evolution of double slots for gift acquisition and digestion (female persistence trait) always occurred when males could not satisfy the demands of females for gifts. However, through coevolutionary reduction in male gift size, fixation of this trait in a population drastically reduced the average female fitness.ConclusionSperm usage patterns, which have rarely been examined for animals with nuptial gifts, can be a critical factor for determining the extent of exaggeration in nuptial gifting. Sex-role reversals in mate competition, as a result of donation of nuptial gifts from males to females, can involve the evolution of male-like, persistent traits in females that reduce population productivity, as is the case with persistence traits in males.

Project description:The knowledge of genetic trends and trade-offs between growth and reproductive traits might be useful to understand the evolution of these traits in livestock and natural populations of animals. We estimated the genetic trends and trade-offs between pre-weaning growth and calving intervals of Nellore animals from a commercial farm. Two-trait animal models were used to estimate covariance components and breeding values (EBV) for direct and maternal genetic effects of pre-weaning growth and direct genetic effects of calving intervals. Regression analyses were performed to examine the relationship between direct and maternal EBV of pre-weaning growth and direct EBV of calving intervals (dependent variables) and the coefficient of generation of each animal (independent variable). We also performed regression analyses to examine the relationship between direct EBV of calving intervals (dependent variables) and direct and maternal EBV of pre-weaning growth (independent variables). The genetic trends for direct and maternal genetic effect for pre-weaning growth were significant and presented genetic evolution in the studied Nellore herd. The genetic trends for the reproductive traits were also significant but indicated genetic changes in an unfavorable way. The genetic correlations between direct effects of pre-weaning growth and calving intervals traits and the genetic correlations between maternal effects of pre-weaning growth traits and direct effects of calving interval traits were not different from zero. The presence of trade-offs between the direct effects of growth and reproductive traits were confirmed through regression from direct EBV of calving intervals over EBV of pre-weaning growth traits. In addition, regression analyses showed that selection to increase pre-weaning growth also increased calving intervals. Our results showed that pre-weaning growth and calving intervals are increasing over generations and that trade-offs occurred between those traits in the studied Nellore herd.

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Is diversification in male reproductive traits driven by evolutionary trade-offs between weapons and nuptial gifts?

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Is diversification in male reproductive traits driven by evolutionary trade-offs between weapons and nuptial gifts?

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