Carlos Cordero

Female choice of sexually antagonistic male adaptations: a critical review of some current research

Abstract We contrast some recent uses of the concept of male‐female conflict, with the type of conflict that is inherent in traditional Darwinian female choice. Females in apparent conflict situations with males may suffer reduced lifetime reproduction, but nevertheless benefit because they obtain sons with superior manipulative abilities. Female defences against male manipulations may not be ‘imperfect’ because of inability to keep pace with male evolution, but in order to screen males and favour those that are especially good manipulators. We examine the consequences of these ideas, and of the difficulties of obtaining biologically realistic measures of female costs, for some recent theoretical and empirical presentations of male–female conflict ideas, and find that male–female conflict in the new sense is less certain than has been commonly supposed. Disentangling previous sexual selection ideas and the new conflict of interest models will probably often be difficult, because the two types of payoffs are not mutually exclusive.

Sexual selection by cryptic female choice on male seminal products - a new bridge between sexual selection and reproductive physiology

Selection clearly focuses on differences in reproduction, but studies of reproductive physiology generally have been carried out in a near vacuum of modern evolutionary theory. This lack of contact between the two fields may be about to change. New ideas indicate that sexual selection by cryptic female choice has affected the evolution of products in male semen that influence female reproductive behavior and physiology.

Sexual conflict and female choice.

Chapman et al. [1] nicely summarize some recent thinking about male–female conflict, but repeat a widespread inconsistency between old and new versions of sexual conflict, and give an overly optimistic impression of support for new models of antagonistic coevolution. They define conflict broadly as ‘differences in the evolutionary interests between males and females’. Such conflict is hardly a new idea. Traditional darwinian sexual selection by female choice [2] inevitably involves male– female conflicts of interest. Chapman et al.’s characterization of the traditional view as ‘one of cooperation and harmony between the sexes’ misreads history. This broad definition contrasts with how the authors propose to distinguish sexual conflict from other models of sexual selection. Here, they emphasize the truly new, but much narrower conflict hypothesis: ‘the force driving the evolution of the [female] preference is better described as a general female avoidance of male-imposed costs, rather than, as in traditional direct models, acquisition of benefits from preferred males’. Inconsistent use of old, broad definitions, and new, narrow definitions has plagued recent literature on sexual conflict. How strong is the support for the new, narrower idea of sexual conflict? Some impressions of conflict, based on observing female ‘resistance’ behavior, or from documenting reproductive costs to females, are misleading [3,4]. A female can gain by being ‘manipulated’ by a male if her indirect gains via increased manipulative abilities of her male offspring are greater than the male-imposed reduction in her own reproduction; under some conditions, female susceptibility to males can be advantageous [4,5]. Chapman et al. argue that such ‘indirect benefits [to the female] are expected to be a weak force in the face of direct selection on preference’, but cite only a theoretical model as evidence. The track record of quantitative conclusions based on mathematical models of sexual selection is rather dismal [2]. Recall, for instance, the now discarded dogma that Fisherian female choice was unlikely because quantitative models had ‘proven’ that there is little or no heritable variability for sexually selected traits in males. The conflicting demonstrations regarding the feasibility of handicap models constitute another example. In addition, empirical evidence indicates that indirect benefits to the female are not necessarily small [6]. Thus, the studies that Chapman et al. cite as documenting the overall cost of manipulation for females, none of which took this possible indirect benefit into account, fail to demonstrate a net cost rather than a net benefit. A second weakness is that costs and benefits cited by Chapman et al. were measured under captive rather than field conditions. It is trite, but nevertheless true [4], that fitness measures made in captivity do not reliably document selection in nature. For instance, reductions in female lifespan in the lab [7] might be irrelevant in nature if females die at earlier ages under natural conditions. Ecological realism is especially important for traits possibly involved in male–female conflict [1], because the demonstration of conflict depends on precise quantitative balancing of costs and benefits. Finally, Chapman et al. do not discuss morphological evidence from many other species that speaks strongly against the importance of new male–female conflict models [8–11].

Interaction Between Sexually Antagonistic Selection and Mate Choice in the Evolution of Female Responses to Male Traits

Theoretical analyses of selection on mutations affecting female responsiveness to male traits suggested that sexually antagonistic selection and traditional female choice are not exclusive alternatives. They can act simultaneously on the same female traits, and can either reinforce or act against each other. These analyses do not yield theoretical predictions regarding the relative frequency and importance of the two types of selection on female responsiveness, as the balance between them is affected by complex factors, including the frequency distribution of male traits, and the mechanisms of male action. Male–female interactions differ from many other evolutionary interactions involving potential evolutionary conflict, in that male and female genomes are irretrievably mixed in their offspring, thus increasing the possibility of indirect payoffs to one participant from the traits of its partner.

Non-resource based territoriality in males of the butterfly Xamia xami (Lepidoptera: Lycaenidae)

In the Pedregal de San Angel reserve, in Mexico City, males of the butterfly Xamia xamiperch in and defend areas with well-defined topographic limits. These areas lack concentrations of receptive females and of larvae and adult resources. One individual defends the same territory an average of 5 h/day, up to a maximum of 23 days. The same areas are used as territories by different males during the year. These areas share some characteristic features which are described. Evidence is presented in support of the hypothesis that the territories function as mating stations. A possible scenario for the evolution of this territorial mating system is advanced.

Multiple mating reduces male survivorship but not ejaculate size in the polygamous insect Stenomacra marginella (Heteroptera: Largidae)

In polygamous species, successful males should be able to inseminate multiple females, to defeat sperm from previous males, to avoid sperm displacement by other males, and to induce females to use his sperm during fertilization. Since resources are limited, adaptations to perform any of these functions may conflict with each other (and with other life-history traits) and trade-offs are expected to evolve. We studied if males of the polygamous true bug Stenomacra marginella face a trade-off between multiple mating and survivorship, by comparing the survivorship of virgin and multiply mated males. We also looked for physiological costs of ejaculate production by examining ejaculate production in consecutive matings in multiple mated males. Multiply mated males were able to produce ejaculates of similar size in up to six consecutive copulations but they had decreased survivorship in comparison with virgin males. There was no difference in survivorship between males mated three and six consecutive times, suggesting that the negative relation between survivorship and number of copulations is not linear. The decrease in survivorship seems to be a cost of mating and ejaculate production. This cost could favor the evolution of prudence in the allocation of resources to ejaculate production (e.g., cryptic male choice).

Are reward polymorphisms subject to frequency‐ and density‐dependent selection? Evidence from a monoecious species pollinated by deceit

Abstract Most deceit‐pollinated species involve floral dimorphisms characterized by the presence of rewarding male flowers and nonrewarding female flowers. It has been proposed that this polymorphism establishes the conditions for the action of frequency dependent selection (FDS). The tendency of foraging animals to aggregate in areas of high resource density suggests that pollination efficiency and fruit production may be positively influenced by flower density (density dependent selection, DDS). In this paper we offer a graphical model describing the effects of FDS and DDS on a monoecious species pollinated by deceit. We test the FDS and DDS assumptions and the predictions of the model using field observations and experimental populations of Begonia gracilis in which population sex ratio and flower density were controlled. We found a marked effect of both FDS and DDS on pollinator visitation, fruit‐set, and on the probability of female flowers to setting fruits. We conclude that these two types of selection have had a strong influence on the evolution of deceit‐pollinated species.

On the Function of Signa, a Genital Trait of Female Lepidoptera

Abstract Female genitalia of insects are formed by several structures whose functions are poorly understood. The signa are sclerotized structures located on the inner wall of the corpus bursa of females of many Lepidoptera species. In this paper, we first describe seven hypotheses concerning the function of signa and derive several predictions from them. Then, we test several of these hypotheses with studies of four butterfly species (Callophrys xami Reakirt, Eueides isabella Cramer, E. lineata Salvin & Godman, and Heliconius ismenius Doubleday) and conclude that in these species signa are mainly used for breaking the envelope of spermatophores. These results are in agreement with the idea that signa are a product of sexual coevolution. Abstract RESUMEN Los genitales femeninos de los insectos están constituidos por varias estructuras cuyas funciones generalmente son poco conocidas. Los signa son estructuras esclerosadas que se localizan en la pared interior del corpus bursa de las hembras de muchas especies de Lepidoptera. En este artículo se describen siete hipótesis sobre la función de los signa y se derivan varias de sus predicciones. Varias de estas hipótesis son evaluadas con estudios realizados con cuatro especies de mariposas (Callophrys xami Reakirt, Eueides isabella Cramer, E. lineata Salvin & Godman, and Heliconius ismenius Doubleday), los cuales llevan a la conclusión de que en estas especies los signa son utilizados principalmente para romper las cubiertas de los espermatóforos. Estos resultados son congruentes con la idea de que los signa son un producto de la coevolución entre machos y hembras.

The evolution of a female genital trait widely distributed in the Lepidoptera: comparative evidence for an effect of sexual coevolution.

Background Sexual coevolution is considered responsible for the evolution of many male genital traits, but its effect on female genital morphology is poorly understood. In many lepidopterans, females become temporarily unreceptive after mating and the length of this refractory period is inversely related to the amount of spermatophore remaining in their genital tracts. Sperm competition can select for males that delay female remating by transferring spermatophores with thick spermatophore envelopes that take more time to be broken. These envelopes could select for signa, sclerotized sharp structures located within the female genital tract, that are used for breaking spermatophores. Thus, this hypothesis predicts that thick spermatophore envelopes and signa evolve in polyandrous species, and that these adaptations are lost when monandry evolves subsequently. Here we test the expected associations between female mating pattern and presence/absence of signa, and review the scant information available on the thickness of spermatophore envelopes. Methodology/Principal Findings We made a literature review and found information on female mating pattern (monandry/polyandry), presence/absence of signa and phylogenetic position for 37 taxa. We built a phylogenetic supertree for these taxa, mapped both traits on it, and tested for the predicted association by using Pagels test for correlated evolution. We found that, as predicted by our hypothesis, monandry evolved eight times and in five of them signa were lost; preliminary evidence suggests that at least in two of the three exceptions males imposed monandry on females by means of specially thick spermatophore envelopes. Previously published data on six genera of Papilionidae is in agreement with the predicted associations between mating pattern and the characteristics of spermatophore envelopes and signa. Conclusions/Significance Our results support the hypothesis that signa are a product of sexually antagonistic coevolution with spermatophore envelopes.

On the function of male genital claspers in Stenomacra marginella (Heteroptera: Largidae)

Male structures for clasping females during precopula interactions and mating (“claspers”) have evolved in many groups of arthropods. Several hypotheses regarding the function of claspers have been proposed. We describe how males of the true bug Stenomacra marginella (Heteroptera: Largidae) move their genital claspers during sexual interactions, and present the results of experiments in which we tested whether claspers are necessary to achieve intromission. When one and both claspers were partially amputated, the probability of successful intromission decreased from 62 to 0% and from 57 to 3%, respectively. Behavioral observations indicate that the claspers open the valves that cover the female genital opening. We consider the possibility that claspers in S. marginella may have multiple functions.