Bias in studies of heterozygosity and mate choice

A key question for molecular and behavioural ecologists who study mating systems is to understand why, in many species, females choose to mate with extra-pair males. Recently a possible explanation, 'genetic compatibility', has gained increasing empirical support (for a comprehensive review, see Kempenaers 2007 ). Genetic compatibility hypotheses assume that females seek extra-pair mates with alleles that complement their own. Typically, this will be achieved by mating with a male of a different genotype than her own, in order to maximise the heterozygosity of her offspring. Because numerous studies have indicated positive associations between heterozygosity and fitness (see Coltman & Slate 2003 ), it follows that mating with 'compatible' males will result in heterozygous, and therefore fit, offspring. Most empirical support for genetic compatibility has been obtained with microsatellite markers that have first been used to assess parentage and then to estimate relatedness and/or individual heterozygosity. A problem with this approach is a possible bias that favours the detection of extra-pair paternity when the extra-pair male has a genotype different from that of the female and her social mate. This in turn could lead to the erroneous conclusion that extra-pair males are less related to the female than within-pair males. In this issue of Molecular Ecology , Wetzel & Westneat 2009 (hereafter W&W), use simulation studies to assess the extent of this bias, using parameter estimates obtained from recent empirical data. They identify two forms of bias that may affect tests of the genetic compatibility hypothesis, and provide guidelines on how these biases may be avoided.     

Breeding experience and the heritability of female mate choice in collared flycatchers

Background

Heritability in mate preferences is assumed by models of sexual selection, and preference evolution may contribute to adaptation to changing environments. However, mate preference is difficult to measure in natural populations as detailed data on mate availability and mate sampling are usually missing. Often the only available information is the ornamentation of the actual mate. The single long-term quantitative genetic study of a wild population found low heritability in female mate ornamentation in Swedish collared flycatchers. One potentially important cause of low heritability in mate ornamentation at the population level is reduced mate preference expression among inexperienced individuals.

Methodology/Principal Findings

Applying animal model analyses to 21 years of data from a Hungarian collared flycatcher population, we found that additive genetic variance was 50 percent and significant for ornament expression in males, but less than 5 percent and non-significant for mate ornamentation treated as a female trait. Female breeding experience predicted breeding date and clutch size, but mate ornamentation and its variance components were unrelated to experience. Although we detected significant area and year effects on mate ornamentation, more than 85 percent of variance in this trait remained unexplained. Moreover, the effects of area and year on mate ornamentation were also highly positively correlated between inexperienced and experienced females, thereby acting to remove difference between the two groups.

Conclusions/Significance

The low heritability of mate ornamentation was apparently not explained by the presence of inexperienced individuals. Our results further indicate that the expression of mate ornamentation is dominated by temporal and spatial constraints and unmeasured background factors. Future studies should reduce unexplained variance or use alternative measures of mate preference. The heritability of mate preference in the wild remains a principal but unresolved question in evolutionary ecology.     

Female within-nest spawning-site preference in a paternal brooding blenny and its effect on the female mate choice

Female spawning-site preference within a nest and its effect on the female mate choice in a paternal brooding blenny Rhabdoblennius ellipes , were examined in rocky intertidal pools using artificial nests. The number of eggs deposited at the nest entrance site was lower than the number deposited at the center and at deep sites. Moreover, the within-nest difference in the egg developmental stage indicated that eggs at the nest entrance site were deposited after those at the center and deep sites. These results indicated that females prefer to spawn eggs in the center and deep sites rather than at the entrance site. Owing to the higher egg mortality rate at the entrance site, females may avoid spawning at such sites. An analysis of the nests in the study area suggested that the within-nest site preference affects female mate choice that is females avoided nests where only the entrance site was available for spawning and instead spawned in nests where the center and deep sites were available.     

The evolution of mate choice and the potential for conflict between species and mate-quality recognition

Understanding how individuals select mates becomes complex when high-quality conspecifics resemble heterospecifics. Individuals facing such a situation may be unable to effectively identify both conspecifics (species recognition) and high-quality mates that can confer fitness benefits to the choosy individual or its offspring (mate-quality recognition). Here I suggest when a conflict may occur between species and mate-quality recognition, discuss the evolutionary consequences stemming from this conflict, and present a model of mate-preference evolution in response to heterospecifics. Determining how species and mate-quality recognition interact to shape mate-choice decisions is important for understanding the diversification of sexually selected traits among closely related taxonomic groups, the use of complex sensory systems for detecting mates, and seemingly inappropriate mate-choice decisions.     

The evolution and significance of male mate choice

The distinct reproductive roles of males and females, which for many years were characterised in terms of competitive males and choosy females, have remained a central focus of sexual selection since Darwin's time. Increasing evidence now shows that males can be choosy too, even in apparently unexpected situations, such as under polygyny or in the absence of male parental care. Here, we provide a synthesis of the theory on male mate choice and examine the factors that promote or constrain its evolution. We also discuss the evolutionary significance of male mate choice and the contrasts in male versus female mate choice. We conclude that mate choice by males is potentially widespread and has a distinct role in how mating systems evolve.     

The evolution of mate choice and mating biases

We review the current status of three well-established models (direct benefits, indirect benefits and sensory drive) and one newcomer (antagonistic chase-away) of the evolution of mate choice and the biases that are expressed during choice. We highlight the differences and commonalities in the underlying genetics and evolutionary dynamics of these models. We then argue that progress in understanding the evolution of mate choice is currently hampered by spurious distinctions among models and a misguided tendency to test the processes underlying each model as mutually exclusive alternatives. Finally, we suggest potentially fruitful directions for future theoretical and empirical research.     

The evolution of postpairing male mate choice

An increasing number of empirical studies in animals have demonstrated male mate choice. However, little is known about the evolution of postpairing male choice, specifically which occurs by differential allocation of male parental care in response to female signals. We use a population genetic model to examine whether such postpairing male mate choice can evolve when males face a trade‐off between parental care and extra‐pair copulations (EPCs). Specifically, we assume that males allocate more effort to providing parental care when mated to preferred (signaling) females, but they are then unable to allocate additional effort to seek EPCs. We find that both male preference and female signaling can evolve in this situation, under certain conditions. First, this evolution requires a relatively large difference in parental investment between males mated to preferred versus nonpreferred females. Second, whether male choice and female signaling alleles become fixed in a population versus cycle in their frequencies depends on the additional fecundity benefits from EPCs that are gained by choosy males. Third, less costly female signals enable both signaling and choice alleles to evolve under more relaxed conditions. Our results also provide a new insight into the evolution of sexual conflict over parental care.     

Testing genetic models of mate choice evolution in the wild

Understanding the mechanisms driving the evolution of mate choice, particularly the importance of indirect genetic benefits, remains a challenge, especially in wild populations. Three recent studies have attempted to quantify the importance of indirect benefits in wild bird populations using approaches derived from quantitative genetic models of mate choice. In all three cases, no support was found for a role of indirect benefits in the evolution of mate choice. These studies suggest that a quantitative genetic approach can illuminate this long-standing problem and that alternative models for the evolution of mate preferences should be tested in wild populations.     

The evolution of mate choice in a fluctuating environment

This paper analyzes the evolutionary dynamics of a locus controlling the degree of female mating preference in a temporally fluctuating environment. Preference for mating with males with respect to their genotypes at a locus that is subject to temporally varying natural selection pressure is considered first. With weak selection and free recombination between the choice locus and the selected locus, preference for mating with heterozygotes appears to be favored. With strong selection, preference for homozygous mates may be favored. In each case, choice alleles may increase from very low initial frequencies to near fixation, in contrast to previous models of mate choice in varying environments. Linkages between the two loci has complex effects on the strength and direction of selection for mate choice. Preference for mating with males with the currently fitter genotypes at the locus under natural selection is also modelled. Provided that the environmental period is not too short, a rare allele conferring such preference may be favored and spread to fixation. Strong natural selection, tight linkage and a short environmental period may produce polymorphism for the level of mate choice.     

The evolution of costly mate choice against segregation distorters

The evolution of female preference for male genetic quality remains a controversial topic in sexual selection research. One well‐known problem, known as the lek paradox, lies in understanding how variation in genetic quality is maintained in spite of natural selection and sexual selection against low‐quality alleles. Here, we theoretically investigate a scenario where females pay a direct fitness cost to avoid males carrying an autosomal segregation distorter. We show that preference evolution is greatly facilitated under such circumstances. Because the distorter is transmitted in a non‐Mendelian fashion, it can be maintained in the population despite directional sexual selection. The preference helps females avoid fitness costs associated with the distorter. Interestingly, we find that preference evolution is limited if the choice allele induces a very strong preference or if distortion is very strong. Moreover, the preference can only persist in the presence of a signal that reliably indicates a male's distorter genotype. Hence, even in a system where the lek paradox does not play a major role, costly preferences can only spread under specific circumstances. We discuss the importance of distorter systems for the evolution of costly female choice and potential implications for the use of artificial distorters in pest control.     

The evolution of female mate choice by sexual conflict

Although empirical evidence has shown that many male traits have evolved via sexual selection by female mate choice, our understanding of the adaptive value of female mating preferences is still very incomplete. It has recently been suggested that female mate choice may result from females evolving resistance rather than attraction to males, but this has been disputed. Here, we develop a quantitative genetic model showing that sexual conflict over mating indeed results in the joint evolution of costly female mate choice and exaggerated male traits under a wide range of circumstances. In contrast to tradition explanations of costly female mate choice, which rely on indirect genetic benefits, our model shows that mate choice can be generated as a side-effect of females evolving to reduce the direct costs of mating.     

Floral evolution and pollinator mate choice in a sexually deceptive orchid

Sexually deceptive orchids mimic sex pheromones and appearance of female insects to attract males, which pollinate the flowers in an attempted mating. This study examines the effects of pollinator mate choice on orchid floral evolution using the Thynnine wasp Neozeleboria cryptoides (Smith) (Hymenoptera: Tiphiidae), which pollinates the sexually deceptive orchid Chiloglottis trapeziformis Fitzg. (i) When male wasps were given the choice between two female dummies of different sizes and identical amount of synthetic pheromone, they preferentially attempted to copulate with medium-sized dummies over small dummies. (ii) When given the choice between two dummies of identical size but different amounts of pheromone, males preferred the larger amount of pheromone. Larger amounts of pheromone generally attracted more males than smaller amounts. (iii) Orchid flower labella, which mimic a female body, were significantly longer and broader than female wasp bodies, and the flowers also produced on average 10 times more 'pheromone' than females. The evolution and maintenance of these exaggerated mating signals is likely to be mediated by the male pollinator behaviour demonstrated here. (iv) When five dummies were offered simultaneously in a 10 cm circular array, males rarely attempted copulation on more than one dummy during a single visit. This behaviour may foster the evolution or maintenance of clonality in C. trapeziformis, as it will minimize pollen exchange within clones.     

Matched filters, mate choice and the evolution of sexually selected traits

Background

Fundamental for understanding the evolution of communication systems is both the variation in a signal and how this affects the behavior of receivers, as well as variation in preference functions of receivers, and how this affects the variability of the signal. However, individual differences in female preference functions and their proximate causation have rarely been studied.

Methodology/Principal Findings

Calling songs of male field crickets represent secondary sexual characters and are subject to sexual selection by female choice. Following predictions from the “matched filter hypothesis” we studied the tuning of an identified interneuron in a field cricket, known for its function in phonotaxis, and correlated this with the preference of the same females in two-choice trials. Females vary in their neuronal frequency tuning, which strongly predicts the preference in a choice situation between two songs differing in carrier frequency. A second “matched filter” exists in directional hearing, where reliable cues for sound localization occur only in a narrow frequency range. There is a strong correlation between the directional tuning and the behavioural preference in no-choice tests. This second “matched filter” also varies widely in females, and surprisingly, differs on average by 400 Hz from the neuronal frequency tuning.

Conclusions/Significance

Our findings on the mismatch of the two “matched filters” would suggest that the difference in these two filters appears to be caused by their evolutionary history, and the different trade-offs which exist between sound emission, transmission and detection, as well as directional hearing under specific ecological settings. The mismatched filter situation may ultimately explain the maintenance of considerable variation in the carrier frequency of the male signal despite stabilizing selection.     

Comparative evaluation and its implications for mate choice

Experiments on decision making by humans show that the choices that we make can be very labile. The magnitude of our preferences, and even our rank ordering of options, can vary according to the number and type of alternatives available for comparison. This apparent irrationality has been argued to result from our use of decision heuristics that have evolved to enable us to choose quickly and efficiently between options differing in multiple attributes. Here, we argue that, because there is also selective pressure for animals to make mating decisions quickly, and because potential mates also differ in multiple attributes, similar decision heuristics might have evolved for mate choice. Following this reasoning, the attractiveness of a given mate will depend on the others with whom he or she is being compared, rather than being an absolute function of his or her underlying quality. We describe some of the ramifications of such comparative evaluation, and argue that it could offer new insights into some of the biggest outstanding problems in mate choice and sexual selection.     

Female mate preference in an invasive phytopathogen vector: how learning may influence mate choice and fecundity in Diaphorina citri

In some arthropods, females learn in the context of reproduction to refine their mate choices and avoid males displaying traits associated with impotency. Previous studies have shown that males of the Asian citrus psyllid, Diaphorina citriKuwayama (Hemiptera: Psyllidae), associate female odor with copulatory rewards. However, it is unclear whether females similarly learn about male traits. We compared mate choice in females previously mated to either blue or orange males and found that females may associate male color with reproductive success, and avoided blue males after previous experience. Orange males mated more frequently than blue males and appeared to be more sexually aggressive in their mating attempts. In addition, females mated to orange males laid approximately twice as many eggs as those mated to blue males. We dissected male psyllids and measured the size of their reproductive organs to determine whether abdominal color was associated with reproductive development. Our morphometric analysis indicated that blue males may not be physiologically immature compared with orange males. Rather, blue males displayed larger testes and seminal vesicles than orange males, suggesting that differences in reproductive output may be behavioral in nature. Based on our data, we suggest that females learn about the appearance and mating behaviors of blue and orange males from early mating experiences, and subsequently avoid blue males in future matings. Although the roles of blue males within a population are unclear, it is possible that blue morphs may specialize in other functions such as dispersal.     

Sexual conflict and the evolution of female mate choice and male social dominance

Conflicts between the sexes over control of reproduction are thought to lead to a cost of sexual selection through the evolution of male traits that manipulate female reproductive physiology and behaviour, and female traits that resist this manipulation. Although studies have begun to document negative fitness effects of sexual conflict, studies showing the expected association between sexual conflict and the specific behavioural mechanisms of sexual selection are lacking. Here we experimentally manipulated the opportunity for sexual conflict in the cockroach. Nauphoeta cinerea and showed that, for this species, odour cues in the social environment influence the behavioural strategies and fitness of males and females during sexual selection. Females provided with the opportunity for discriminating between males but not necessarily mating with preferred males produced fewer male offspring than females mated at random. The number of female offspring produced was not affected, nor was the viability of the offspring. Experimental modification of the composition of the males' pheromone showed that the fecundity effects were caused by exposure to the pheromone component that makes males attractive to females but also makes males less likely to be dominant. Female mate choice therefore carries a demographic cost but functions to avoid male manipulation and aggression. Male-male competition appears to function to circumvent mate choice rather than directly manipulating females, as the mate choice can be cryptic. The dynamic struggle between the sexes for control of mating opportunities and outcomes in N. cinerea therefore reveals a unique role for sexual conflict in the evolution of the behavioural components of sexual selection.     

The evolution of parent–offspring conflict over mate choice

In human societies, parents often have a strong influence on the mate choice of their offspring. Moreover, empirical studies show that conflict over mate choice between parents and offspring is widespread across human cultures. Here we provide the first theoretical investigation into this conflict, showing that it may result from an underlying evolutionary conflict over parental resource distribution. We present a series of evolutionary simulations in which we gradually expand a standard model of sexual selection by the stepwise addition of elements of parental involvement. In our model, females obtain resources enhancing their fecundity from both their chosen mate and their parents. Potential mates differ in their ability to provide resources and may signal this ability. Both females and their parents can develop a preference for the signal, with both preferences influencing the realized mate choice of the female. Parents may differentially allocate resources among their daughters depending on the resource-provisioning abilities of their sons-in-law. When fecundity returns on investment are diminishing, we find that parents invest most in daughters whose mates provide few resources. Subsequently, the daughters evolve to exploit this allocation rule through their mate choice, which is not in the parents' best interests. This results in a conflict over mate choice between parents and their offspring, manifested as an on-going divergence of offspring and parental preferences. We predict that the conflict should be most pronounced when fathers, as opposed to mothers, control resource allocation.     

Fluctuating environments, sexual selection and the evolution of flexible mate choice in birds

Environmentally-induced fluctuation in the form and strength of natural selection can drive the evolution of morphology, physiology, and behavior. Here we test the idea that fluctuating climatic conditions may also influence the process of sexual selection by inducing unexpected reversals in the relative quality or sexual attractiveness of potential breeding partners. Although this phenomenon, known as 'ecological cross-over', has been documented in a variety of species, it remains unclear the extent to which it has driven the evolution of major interspecific differences in reproductive behavior. We show that after controlling for potentially influential life history and demographic variables, there are significant positive associations between the variability and predictability of annual climatic cycles and the prevalence of infidelity and divorce within populations of a taxonomically diverse array of socially monogamous birds. Our results are consistent with the hypothesis that environmental factors have shaped the evolution of reproductive flexibility and suggest that in the absence of severe time constraints, secondary mate choice behaviors can help prevent, correct, or minimize the negative consequences of ecological cross-overs. Our findings also illustrate how a basic evolutionary process like sexual selection is susceptible to the increasing variability and unpredictability of climatic conditions that is resulting from climate change.