Evolution of nuptial gifts and its coevolutionary dynamics with male-like persistence traits of females for multiple mating

Abstract Background Many 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...

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Main Authors: Yoshitaka Kamimura, Kazunori Yoshizawa, Charles Lienhard, Rodrigo L. Ferreira, Jun Abe
Format: Article
Language:English
Published: BMC 2021-09-01
Series:BMC Ecology and Evolution
Subjects:
Online Access:https://doi.org/10.1186/s12862-021-01901-x
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spelling doaj-a6d55beb8ece4f69b6e2bd01fbc026dc2021-09-12T11:04:13ZengBMCBMC Ecology and Evolution2730-71822021-09-0121111410.1186/s12862-021-01901-xEvolution of nuptial gifts and its coevolutionary dynamics with male-like persistence traits of females for multiple matingYoshitaka Kamimura0Kazunori Yoshizawa1Charles Lienhard2Rodrigo L. Ferreira3Jun Abe4Department of Biology, Keio UniversitySystematic Entomology, School of Agriculture, Hokkaido UniversityGeneva Natural History MuseumBiology Department, Federal University of LavrasFaculty of Liberal Arts, Meijigakuin UniversityAbstract Background Many 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. Results Our 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. Conclusion Sperm 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.https://doi.org/10.1186/s12862-021-01901-xNuptial giftPaternity determination mechanismCoevolutionFemale persistence traitFemale penisSex role reversal
collection DOAJ
language English
format Article
sources DOAJ
author Yoshitaka Kamimura
Kazunori Yoshizawa
Charles Lienhard
Rodrigo L. Ferreira
Jun Abe
spellingShingle Yoshitaka Kamimura
Kazunori Yoshizawa
Charles Lienhard
Rodrigo L. Ferreira
Jun Abe
Evolution of nuptial gifts and its coevolutionary dynamics with male-like persistence traits of females for multiple mating
BMC Ecology and Evolution
Nuptial gift
Paternity determination mechanism
Coevolution
Female persistence trait
Female penis
Sex role reversal
author_facet Yoshitaka Kamimura
Kazunori Yoshizawa
Charles Lienhard
Rodrigo L. Ferreira
Jun Abe
author_sort Yoshitaka Kamimura
title Evolution of nuptial gifts and its coevolutionary dynamics with male-like persistence traits of females for multiple mating
title_short Evolution of nuptial gifts and its coevolutionary dynamics with male-like persistence traits of females for multiple mating
title_full Evolution of nuptial gifts and its coevolutionary dynamics with male-like persistence traits of females for multiple mating
title_fullStr Evolution of nuptial gifts and its coevolutionary dynamics with male-like persistence traits of females for multiple mating
title_full_unstemmed Evolution of nuptial gifts and its coevolutionary dynamics with male-like persistence traits of females for multiple mating
title_sort evolution of nuptial gifts and its coevolutionary dynamics with male-like persistence traits of females for multiple mating
publisher BMC
series BMC Ecology and Evolution
issn 2730-7182
publishDate 2021-09-01
description Abstract Background Many 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. Results Our 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. Conclusion Sperm 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.
topic Nuptial gift
Paternity determination mechanism
Coevolution
Female persistence trait
Female penis
Sex role reversal
url https://doi.org/10.1186/s12862-021-01901-x
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