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 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.

Acquisition of novel muscles enabled protruding and retracting mechanisms of female penis in sex-role reversed cave insects

“…In addition, active competition for seminal nutrition by females has also been observed in other trogiomorphans [2,27]. The most likely explanation is that the modification of the spermapore plate toward the female penis was promoted by sexual selection to receive more seminal nutrition [2,6]. The shaft and associated muscles in the non-protruding prepenis of Sensitibilla are also expected to have functions increasing the female's benefit, such as stimulation of the male mate in order to receive more nutritious semen.…”

“…The reversals of male and female genital function require complete correlation between the sexes, and the evolution of such anomalies must be strongly constrained [2]. The oligotrophic cave environment [4] and seminal nuptial gift [1] are thought to be the key factors facilitating female competition and, as a consequence, the origin of the female penis [5,6]. In addition, females of Neotrogla have multiple sperm storages (twin insemination slots with switching valve to receive twice the amount of nutritious seminal gift at the same time) [7].…”

“…In addition, females of Neotrogla have multiple sperm storages (twin insemination slots with switching valve to receive twice the amount of nutritious seminal gift at the same time) [7]. This unique feature renders female–female competition more intense, favouring the evolution of a female penis [2,6,8].…”

A general model for the evolution of nuptial gift-giving

“…Recent studies have modelled some frequency-dependent aspect of nuptial gift giving using evolutionary game theory 20,21 . Two such studies formulated a quantitative genetics model to study evolutionarily stable nuptial gifts sizes in populations where the female propensity to remate was evolving 4,5 . The results obtained in these studies complement our results by giving equilibrium solutions to the evolutionary stable nuptial gift size, whereas we determine the general conditions under which nuptial gift-giving will evolve as given by the inequalities we derive.…”

“…Despite the ubiquity of this behaviour, little effort has been made to conceptualise the evolution of nuptial gift-giving within a general modelling framework 1,4 . Recent models describing the evolution of nuptial gift-giving have focused on co-evolution between male nuptial gift-giving and female propensity to remate, and the evolutionarily stable nuptial gift sizes 4,5 , but a general framework describing the conditions necessary for nuptial gift-giving to be initially favoured by selection is needed to understand when gift-giving should evolve. Nuptial gift-giving may allow males to increase fitness by acquiring additional mates, indirect benefits (by increasing the fitness of offspring), prolonged copulations, and success in sperm competition 1,6,7 .…”