Female mate preferences in Drosophila simulans: evolution and costs

Female mate preference is central to sexual selection, and all indirect benefit models require that there is genetic variation in female preference. This has rarely been tested however, with relatively few studies documenting heritable variation in female preference and even fewer that have directly selected on mate preference to unequivocally show that it can evolve. Additionally, costs of mate preference are poorly understood even though these have implications for preference evolution. We selected on female preference for ebony‐males in replicate Drosophila simulans lines, and generated a rapid evolutionary response in both replicates, with the proportion of females mating with ebony‐males increasing from approximately 5% to 30% after five generations of selection. This increase was independent of changes in ebony‐males as only females were included in our selection regime. We could detect no cost to mate preference itself other than that associated with the fitness consequences of mating with ebony males.     

Crypsis hypothesis as an explanation for evolution of impermeable coats in seeds is anecdotal

Impermeable seed/fruit coat, i.e. physical dormancy (PY) occurring in seeds of many genera of 19 angiosperm plant families has been traditionally viewed as a form of dormancy that regulates germination timing. However, this view was recently challenged by an alternative explanation claiming that the impermeable seed coat evolved as a coping mechanism to escape predators, i.e. crypsis hypothesis. Here, I wish to call for more careful attention on crypsis as an evolutionary factor because (1) information of volatile compounds is not known in PY families except Fabaceace; (2) impermeability is not induced until the moisture content of the seeds drops below species-specific threshold suggesting that drying determines development of impermeable seed coats; (3) the crypsis hypothesis does not explain the year-to-year or between site variations in proportions of impermeable seeds produced by plants; and (4) dry seeds of species from non-PY families also do not emit volatile compounds, and do not develop impermeable seed coats. For these reasons, it appears crypsis might be an exaptation, i.e., a trait that performs a function for which it was not originally evolved. Based on the available evidence, it is suggested that climate drying might have resulted in evolution of impermeable seed coats.     

Genetic niche-hiking: an alternative explanation for the evolution of flammability

In fire-prone ecosystems, many plants possess traits that enhance their relative flammability and ecologists have suggested increased flammability could result from natural selection. To date, theoretical models addressing the evolution of flammable characteristics assume that flammable plants realize some direct fitness advantage. In this paper, we explore the idea that enhanced flammability can increase in frequency in a population without any direct fitness benefit to the flammable type. In our model, flammability evolves due to an association between an allele that promotes flammability and alleles at unlinked loci that give high fitness. In analogy to genetic hitchhiking, in which a deleterious allele can invade due to a genetic linkage, we call this process "genetic niche-hiking," because the association results from localized niche construction. Specifically, flammable plants sacrifice themselves and their neighbors to produce local fire-cleared gaps (the constructed niche) in which their offspring are able to continually track an ever-changing environment. Niche-hiking requires that mating, dispersal and niche construction all occur locally (i.e. the population is spatially structured), such that offspring are likely to experience the niches their parents construct. Using a spatially-explicit lattice-based simulation, we find that increased flammability can evolve despite the "self-killing" cost of such a trait. Genetic niche-hiking may also be applicable to the evolution of other traits in spatially structured ecological systems such as plant disease susceptibility and forest tree characteristics that influence gap production.     

Genetic explanation for vertical evolution

The genetic theory of natural selection proposed by Fisher takes into account differential reproduction success of organisms, which may be estimated by using the Malthusian parameter as fitness. However, the minimum possible value of this parameter depends on ecological stability of an organism, which determines the probability of the survival and participation in reproduction for each viable offspring. In the course of vertical evolution, leading to an increase in the level of biological organization, ecological stability of organisms increases, and this might be accompanied by a decrease in their fitness. In the macroevolutionary process, alterations in ecological stability of organisms, including those responsible for an increase in the level of biological organization, are basic and primary changes whereas alterations in fitness are additional and secondary.     

The genetic basis of female mate preferences

We review the evidence for genetic variation in female and male mate preferences. Genetic differences between species and partially isolated races show that preferences can evolve and were genetically variable in the past. Within populations there is good evidence of genetic variation, both of discrete genetic effects (8 cases) and quantitative genetic effects (17 cases), from a diverse range of taxa. We also review evidence for the presence of genetic covariance between mate preferences and sexual traits in the other sex. The 11 studies go a long way to validating the theoretical prediction of positive genetic covariance. The few negative results are best explained by a lack of appropriate experimental design. One unresolved question is whether genetic covariance is due to linkage disequilibrium between unlinked genes or physical linkage. Some evidence points to linkage disequilibrium but this is not yet conclusive.     

Snorkeling preferences foster an amino acid composition bias in transmembrane helices

By analyzing transmembrane (TM) helices in known structures, we find that some polar amino acids are more frequent at the N terminus than at the C terminus. We propose the asymmetry occurs because most polar amino acids are better able to snorkel their polar atoms away from the membrane core at the N terminus than at the C terminus. Two findings lead us to this proposition: (1) side-chain conformations are influenced strongly by the N or C-terminal position of the amino acid in the bilayer, and (2) the favored snorkeling direction of an amino acid correlates well with its N to C-terminal composition bias. Our results suggest that TM helix predictions should incorporate an N to C-terminal composition bias, that rotamer preferences of TM side-chains are position-dependent, and that the ability to snorkel influences the evolutionary selection of amino acids for the helix N and C termini.     

Heterosis as an explanation for large amounts of genic polymorphism

By using both numerical and analytical approaches, we have shown that heterosis alone is not a mechanism for maintaining many alleles segregating at a locus. Even when all heterozygous are more fit than all homozygotes, the proportion of fitness arrays that will lead to a stable, feasible equilibrium of more than 6 or 7 alleles is vanishingly small. More alleles can be maintained if, in addition to heterosis, it is assumed that there is very little variation in fitness from heterozygote to heterozygote, with the ratio of mean heterosis to standard deviation of fitness among heterozygotes in the neighborhood of 10. When such conditions hold, the allelic frequency distribution and equilibrium will be very uniform, with all alleles very close to equal frequency (see PDF). It is much more likely that stable equilibria for multiple alleles will be best explained by multiple niche selection.     

Change of type as an explanation for the decline of therapeutic bloodletting

In clinical lectures given between 1850 and 1852, William Pultney Alison, a senior Edinburgh physician, reflected on whether therapeutic bloodletting could be useful in some cases of pneumonia but harmful in others. If so, Alison reasoned, a change in the form of the disease—a change of type—could explain why therapeutic bloodletting had been nearly abandoned in treating a disease for which, only a few years earlier, it had been the standard therapy. In response, a young pathologist, John Hughes Bennett, denied that anything like a change of type had occurred and insisted that bloodletting had never been an effective therapy. Over the next two decades, more than forty physicians debated the usefulness of bloodletting and the reasons for its decline. This debate, known as the Edinburgh Bloodletting Controversy, has attracted the attention of contemporary historians. Those who have discussed the debate side with Bennett and give Alison little serious attention. I argue that by examining the texts to determine what the issues really were, we can see that Alison may actually have been right. Moreover, this examination illuminates the practice of bloodletting and reveals one hitherto unrecognized factor that contributed to its decline.     

A receiver bias in the origin of three-spined stickleback mate choice

Receiver-bias models of signal evolution predict that male sexually selected traits evolve through prior selection for other functions. Female three-spined sticklebacks (Gasterosteus aculeatus) in many populations show a mating preference for males with a red throat and jaw. It has been proposed that this preference evolved because the choice of males with red coloration confers direct and indirect benefits to females in accordance with the Fisher-Zahavi model of sexual selection. We present indirect evidence that the preference is an effect of a receiver bias in the perceptual or cognitive system of G. aculeatus for the colour red, which may have arisen in the context of foraging. In laboratory trials, male and female three-spined and nine-spined sticklebacks (Pungitius pungitius) responded most strongly to red objects outside a mating context. This result demonstrates a correlation between a sexually selected trait and an intrinsic attraction to red objects, and supports the sensory-exploitation model for the evolution of red nuptial coloration in three-spined sticklebacks.     

Character displacement and the evolution of mate choice: an artificial neural network approach

Interactions with heterospecifics can promote the evolution of divergent mating behaviours between populations that do and do not occur with heterospecifics. This process--reproductive character displacement--potentially results from selection to minimize the risk of mating with heterospecifics. We sought to determine whether heterospecific interactions lead to divergence of female preferences for aspects of conspecific male signals. We used artificial neural network models to simulate a mate recognition system in which females co-occur with different heterospecifics in different populations. Populations that evolved conspecific recognition in the presence of different heterospecifics varied in their preferences for aspects of conspecific male signals. When we tested networks for their preferences of conspecific versus heterospecific signals, however, we found that networks from allopatric populations were usually able to select against heterospecifics. We suggest that female preferences for aspects of conspecific male signals can result in a concomitant reduction in the likelihood that females will mate with heterospecifics. Consequently, even females in allopatry may discriminate against heterospecific mates depending on the nature of their preferences for conspecifics. Such a pattern could potentially explain cases where reproductive character displacement is expected, but not observed.     

A simple and general explanation for the evolution of altruism

We present a simple framework that highlights the most fundamental requirement for the evolution of altruism: assortment between individuals carrying the cooperative genotype and the helping behaviours of others with which these individuals interact. We partition the fitness effects on individuals into those due to self and those due to the 'interaction environment', and show that it is the latter that is most fundamental to understanding the evolution of altruism. We illustrate that while kinship or genetic similarity among those interacting may generate a favourable structure of interaction environments, it is not a fundamental requirement for the evolution of altruism, and even suicidal aid can theoretically evolve without help ever being exchanged among genetically similar individuals. Using our simple framework, we also clarify a common confusion made in the literature between alternative fitness accounting methods (which may equally apply to the same biological circumstances) and unique causal mechanisms for creating the assortment necessary for altruism to be favoured by natural selection.     

Female mate preferences and subsequent resistance to copulation in the mallard

In the majority of socially monogamous bird species, femalessolicit or accept copulations from males other than their partner.Females may gain direct benefits from extrapair males, suchas greater access to resources, or indirect genetic benefitsthat will influence the future success of their offspring. However,one group of birds appears to be the exception to this generalrule; in the wildfowl (Anseriformes), all extrapair copulationsappear to be resisted by females. It has been suggested thatresistance behavior may be a strategy to allow females a greaterchoice of mates, either at the precopulatory level (to promotechoice of copulation partner) and/or the postcopulatory level(to promote multiple mating to increase their choice of sperm).This paper examines the function of female resistance behaviorin one of the dabbling ducks, the mallard (Anas platyrhynchos).Observations on a marked population of wild mallard and experimentswith captive birds found that although females showed a strongpreference for particular males that are the first to molt intotheir breeding plumage, male attractiveness did not influencefemale responses to pair or extrapair copulation attempts. Femaleresistance decreased the likelihood that copulation attemptswould end in successful insemination. The findings did not supportthe hypothesis that females resist copulations to promote femalechoice and the reasons why waterfowl may benefit from avoidingall extrapair copulations are discussed.     

Relationship of serum testosterone concentrations to mate preferences in rams

This study examined systemic testosterone concentrations in rams that were classified according to their sexual behavior and partner preference as either female-oriented (FOR), male-oriented (MOR), or asexual (NOR). For this purpose, we measured testosterone concentrations under three separate conditions: in conscious rams during the nonbreeding season (June) and breeding season (November), and in anesthetized rams during the breeding season. Basal testosterone concentrations in conscious rams were not different among the three groups (P > 0.05) in either season. However, when rams were anesthetized, mean systemic concentrations of testosterone in FORs (mean +/- SEM, 13.9 +/- 7.4 ng/ml serum) were greater (P < 0.05) than in NORs (0.9 +/- 0.1 ng/ml), but not in MORs (2.2 +/- 6.2 ng/ml), whereas testosterone concentrations were not different between MORs and NORs (P > 0.05). Concentrations of testosterone in the spermatic vein of FORs (127 +/- 66 ng/ml) were greater (P < 0.05) than in MORs (41 +/- 10 ng/ml) and NORs (19 +/- 7 ng/ml). Serum LH concentrations were not different. Cortisol was higher (P < 0.05) in anesthetized MORs (25.1 +/- 4.2 ng/ml) and NORs (27.2 +/- 4.4 ng/ml) than in FORs (10.9 +/- 1.8 ng/ml). These results demonstrate that circulating testosterone concentrations are related to sexual behavior only when rams are bled under anesthesia. Thus, differences in basal androgen concentrations in adulthood cannot be responsible for expression of male-oriented preferences or low libido in sheep. Instead, functional differences must exist between the brains of rams that differ in sexual preference expression.     

The health of a nation predicts their mate preferences: cross-cultural variation in women's preferences for masculinized male faces

Recent formulations of sexual selection theory emphasize how mate choice can be affected by environmental factors, such as predation risk and resource quality. Women vary greatly in the extent to which they prefer male masculinity and this variation is hypothesized to reflect differences in how women resolve the trade-off between the costs (e.g. low investment) and benefits (e.g. healthy offspring) associated with choosing a masculine partner. A strong prediction of this trade-off theory is that women''s masculinity preferences will be stronger in cultures where poor health is particularly harmful to survival. We investigated the relationship between women''s preferences for male facial masculinity and a health index derived from World Health Organization statistics for mortality rates, life expectancies and the impact of communicable disease. Across 30 countries, masculinity preference increased as health decreased. This relationship was independent of cross-cultural differences in wealth or women''s mating strategies. These findings show non-arbitrary cross-cultural differences in facial attractiveness judgements and demonstrate the use of trade-off theory for investigating cross-cultural variation in women''s mate preferences.     

Kleptoparasitism as an explanation for paradoxical oviposition decisions of the parasitoid Asobara tabida

It is known that the braconid Asobara tabida, a parasitoid of Drosophila larvae, takes oviposition decisions in accordance with survival probabilities in several host species. Nevertheless, larvae of D. simulans, in which the survival probability is virtually zero, are readily accepted for oviposition by searching females. This even happens when they are offered together with D. melanogaster larvae, in which the parasitoid can develop. Here I show that A. tabida can act as a kleptoparasitoid in D. simulans larvae: it can develop in D. simulans larvae, once these larvae are parasitized by another parasitoid, the eucoilid Leptopilina boulardi. Analysis with an optimal foraging model suggests that the increase in survival probability and the occurrence of L. boulardi in the field are high enough to make this kleptoparasitic behaviour of A. tabida pay.     

Generalization and the evolution of symmetry preferences

Biological displays are often symmetrical, and there is growing evidence that receivers are sensitive to these symmetries. One explanation for the evolution of such sensitivity is that symmetry reflects the quality of the signaller. An alternative is that the sensitivity may arise as a by-product of general properties of biological recognition systems. In line with the latter idea, simulations of the recognition process based on simple, artificial neural networks have suggested that generalization can give rise to preferences for particular symmetrical stimuli. However, it is not clear from these studies exactly how the preferences emerge, and to what extent the results are relevant to biological recognition systems. Here, we employ a different class of recognition models (gradient interaction models) to demonstrate more clearly how generalization can generate a preference for symmetrical variants of a display. We also point out that the predictions of the gradient interaction and network-based models regarding the effects of generalization closely match the results from empirical studies of stimulus control. Our analysis demonstrates that the effects of generalization cannot be ignored when studying the evolution of symmetry preferences and symmetric signals.