The evolution of male and female mating preferences in Drosophila speciation*

The relative importance of male and female mating preferences in causing sexual isolation between species remains a major unresolved question in speciation. Despite previous work showing that male courtship bias and/or female copulation bias for conspecifics occur in many taxa, the present study is one of the first large‐scale works to study their relative divergence. To achieve this, we used data from the literature and present experiments across 66 Drosophila species pairs. Our results revealed that male and female mate preferences are both ubiquitous in Drosophila but evolved largely independently, suggesting different underlying evolutionary and genetic mechanisms. Moreover, their relative divergence strongly depends on the geographical relationship of species. Between allopatric species, male courtship and female copulation preferences diverged at very similar rates, evolving approximately linearly with time of divergence. In sharp contrast, between sympatric species pairs, female preferences diverged much more rapidly than male preferences and were the only drivers of enhanced sexual isolation in sympatry and Reproductive Character Displacement (RCD). Not only does this result suggest that females are primarily responsible for such processes as reinforcement, but it also implies that evolved female preferences may reduce selection for further divergence of male courtship preferences in sympatry.     

Inheritance features of mating behavior components in Drosophila melanogaster and their significance for fitness

Components of mating behavior of Drosophila melanogaster mutant and wild-type strains were studied with respect to fitness. The magnitude of the effect of genotype on the male mating activity, female sexual receptivity, fertility and viability was determined. Strong positive correlation was found between the male mating activity and fitness components. It was shown that mating of strains contrasting in sexual behavior features can be accompanied by both heterosis and maternal effect. Inheritance coefficients were determined for sexual behavior components.     

The evolution of polyandry: multiple mating and female fitness in insects

Theory suggests that male fitness generally increases steadily with mating rate, while one or a few matings are sufficient for females to maximize their reproductive success. Contrary to these predictions, however, females of the majority of insects mate multiply. We performed a meta-analysis of 122 experimental studies addressing the direct effects of multiple mating on female fitness in insects. Our results clearly show that females gain directly from multiple matings in terms of increased lifetime offspring production. Despite a negative effect of remating on female longevity in species without nuptial feeding, the positive effects (increased egg production rate and fertility) more than outweigh this negative effect for moderate mating rates. The average direct net fitness gain of multiple mating was as high as 30-70%. Therefore, the evolutionary maintenance of polyandry in insects can be understood solely in terms of direct effects. However, our results also strongly support the existence of an intermediate optimal female mating rate, beyond which a further elevated mating rate is deleterious. The existence of such optima implies that sexual conflict over the mating rate should be very common in insects, and that sexually antagonistic coevolution plays a key role in the evolution of mating systems and of many reproductive traits. We discuss the origin and maintenance of nuptial feeing in the light of our findings, and suggest that elaborate and nutritional ejaculates may be the result of sexually antagonistic coevolution. Future research should aim at gaining a quantitative understanding of the evolution of female mating rates. Copyright 2000 The Association for the Study of Animal Behaviour.     

蛾类雄虫交配史对雌虫生殖适合度的影响:Meta分析

本文利用Meta分析方法,从29篇实例研究性文献中对27种雌性蛾类的适合度参数(产卵量、孵化率和寿命)进行分析,以确定雄虫的交配史如何影响雌虫的生殖适合度以及这种影响是否受科属和交配策略的影响。结果表明:雄虫的交配史对自身的精包大小或精子数量以及雌虫的生殖适合度具有明显的负作用,且这种负作用明显受科属和交配策略的影响;在菜蛾科、草螟科、螟蛾科、潜蛾科和蓑蛾科中,与有交配经历的雄虫交配后,雌蛾产卵量明显下降,但在卷蛾科和夜蛾科中没有差异;在潜蛾科、蓑蛾科、卷蛾科和夜蛾科中,与有交配经历的雄虫交配后,雌蛾卵孵化率明显下降,但在菜蛾科、草螟科和螟蛾科中没有差异;草螟科和螟蛾科中的雌蛾寿命随雄蛾的交配史而缩短,而卷蛾科和夜蛾科的雌蛾寿命随配偶的交配史而明显增加;尽管雄蛾交配史对单配制和多配制雌蛾的产卵量和孵化率具有明显的负作用,但雄虫的交配史明显缩短了单配制雌蛾的寿命而延长了多配制雌蛾的寿命;因此我们认为,在蛾类昆虫中,雄虫的交配史是影响雌虫生殖适合度的关键因素之一。     

多次交配对雌性蛾类生殖适应性影响的Meta分析

多次交配是昆虫中一种重要的交配行为,许多学者对此开展了大量的研究以解释雌性昆虫多次交配行为的适应性意义。在鳞翅目蛾类昆虫中存在两种典型的交配策略(单配制和多配制),但这两类交配策略的雌蛾进行多次交配获得哪些利益和代价目前仍不清楚。本文采用Meta分析法对搜集到的24篇文献中来自8科25种蛾类进行分析,比较两种不同交配策略的雌蛾多次交配与其适应性参数之间的关系。结果表明,多次交配行为明显增加了雌蛾的产卵量和卵的孵化率,而导致寿命的下降。其中,多次交配导致多配制蛾类产卵量和卵的孵化率明显的增加,但寿命趋于延长却没有明显差异;而对单配制蛾类而言,多次交配对相应的适应性参数均没有明显的影响。     

Repetitive mating and female fitness in Dysdercus cardinalis (Hemiptera: Pyrrhocoridae)

Using three mating-treatment groups–pairing with a male for life, pairing with a male from adult emergence to first oviposition, and no pairing (virgin)–of Dysdercus cardinalis females in a laboratory study, the following results were obtained. Most of the virgin females did not lay eggs; those that did oviposited for the first time at a considerably older age than females in the other two groups. In a lifetime, females pairing with a male for life and those pairing with a male up to first oviposition produced essentially the same number of eggs, and this was more than 3.5 times the number of eggs laid by a virgin female. Virgin females produced an average of 1.3 clutches in a lifetime, compared with about 4.5 clutches produced by females in the other two groups. Reproductive span was significantly shorter, and fecundity per day of reproductive span significantly greater, for females pairing with males for life than for those pairing with a male up to first oviposition. Age at death was significantly different amongst females in different mating-treatment groups. Virgin females had the longest life, followed by females pairing with a male up to first oviposition and females pairing with a male for life, in that order. There was a positive correlation between lifetime gross reproduction and age at death for females pairing with a male for life. There was no relationship between these two characters for females pairing with a male up to first oviposition. Both females pairing with a male for life and those pairing with a male to first oviposition exhibited a significant inverse relationship between fecundity per day and age at death. The results obtained indicate that (1) mating is a prerequisite for normal gonadal activity in Dysdercus cardinalis , and (2) repetitive mating increases the rate of reproduction. This would reduce the mean age of parenthood which is inversely related to the intrinsic rate of increase.     

The effect of mating frequency and mating pattern on female reproductive fitness in cabbage beetle,Colaphellus bowringi

It is generally thought that females can receive more of the material benefits from males by increasing mating frequency and polyandry can lead to greater reproductive success. The cabbage beetle, Colaphellus bowringi Baly (Coleoptera: Chrysomelidae), is a highly promiscuous species, in which females or males can readily mate repeatedly with a given partner or multiple partners at a very high frequency. In the present study, the effect of mating frequency (number of matings) and mating pattern (polyandry vs. monogamy) on female reproductive fitness was investigated by measuring fecundity, fertility, and female longevity. The results indicated that increased female mating frequency with the same male did not result in variation in lifetime fecundity, but significantly increased fertility and decreased female longevity. Moreover, five copulations were sufficient to acquire maximal reproductive potential. Female lifetime fecundity also did not differ between polyandrous and monogamous treatments. However, monogamous females exhibited a significant increase in fertility and significant prolongation of longevity compared with polyandrous females, further demonstrating that monogamy is superior to polyandry in this beetle.     

Evidence for minority male mating success and minority female mating disadvantage in Drosophila ananassae

Frequency-dependent mating success was tested for three pairs of wild-type and mutant strains of Drosophila ananassae, MY and yellow body color (y), PN and claret eye color (ca), and TIR and cut wing (ct). The two strains of each pair were chosen for their approximately equal mating propensities. Multiple-choice experiments, using different experimental procedures, were employed. The tests were carried out by direct observation in Elens-Wattiaux mating chambers with five different sex ratios (4:16, 8:12, 10:10, 12:8, and 16:4). There was no assortative mating and sexual isolation between the strains, based on 2 x 2 contingency chi2 analysis and isolation estimate values. One-sided rare male mating advantages were found in two experiments, one for ca males and the other for wild-type males (TIR). However, no advantage was found for rare males in the experiment with MY and y flies. Mating disadvantages for rare females were found for sex-linked mutants (y and ct). Two different observational methods (removal or direct observation of mating pairs) imparted no overall significant effects on the outcome of the frequency-dependent mating tests.     

Pole cells of Drosophila paulistorum: embryologic differentiation with symbionts.

The pole cells of young D. paulistorum embryos are destined to form the germinal cells of both male and female imagoes. In addition, specialized portions of the midgut may be derived from pole cell progenitors. In this initial study of their embryogenesis by means of electron microscopy, various stages of pole cell development are shown in both non-hybrid (potentially fertile) and intersemispecific hybrid (potentially sterile as males) materials. Originally, approximately 5 or 6 cells emerge to form the early polar cap and subsequently divide asynchronously until the 35-50 cells of the late polar cap are derived. Unlike other Drosophila species, however, mycoplasma-like symbionts, apparently an hereditary infection, have been traced to locations within the cytoplasm of these pole cells. They are depicted as arriving there after transmission via the egg cytoplasm, implicating this as their probable route of entry into the future germinal tissues of adult flies. It is postulated that these microorganisms function as an infectious reproductive isolating mechanism fostering hybrid male sterility between D. paulistorum semispecies.     

The impact of extra-pair mating behavior on hybridization and genetic introgression

Hybridization and genetic introgression can be associated with secondary contact between closely related species. Previous models have examined the ecological and demographic conditions leading to hybridization and introgression, but few have examined the role of behavior. Alternative mating behaviors are common throughout the animal kingdom but have rarely been recognized as a potential mechanism for hybridization. We developed an individual-based genetic model to examine the hypothesis that extra-pair copulations (EPCs) can lead to hybridization and genetic introgression even when assortative mating preferences are intact. Our model showed that female choice, whether pre- or post-copulation, reinforced species boundaries and that hybrids were relatively uncommon when no EPCs occurred. However, when EPCs were introduced into the model, the proportion of hybrids in the population depended on the strength of female mate or sperm choice, the strength of male pursuit of EPCs, and habitat-induced effects on the species composition of the neighborhood. As predicted, male pursuit of EPCs caused extensive introgression, but female preference for conspecific paternity reinforced species differences. Inclusion of mitochondrial markers of species identity revealed significant effects of interspecific and intersexual behavior during EPCs on the direction of introgression. These results suggest that an alternative mating tactic may have major effects on the level of genetic homogenization and can cause local extinction of a species.     

Influence of female age, sperm senescence and multiple mating on sperm viability in female Drosophila melanogaster

Sperm viability has been associated with the degree of promiscuity across species, as well as the degree of reproductive success within species. Thus, sperm survival within the female reproductive tract likely plays a key role in how mating systems evolve. In the fruit fly, Drosophila melanogaster, however, the extent and cause of sperm death has been the subject of recent debate. Here, we assess sperm death within the female reproductive tract of D. melanogaster following single and multiple matings in order to elucidate the extent of death and its potential mechanisms, including an acute female response to mating, female age and/or sperm senescence. We found no evidence that sperm viability was influenced by an acute female response or female age. We also found that rival ejaculates did not influence viability, supporting recent work in the system. Instead, the majority of death appears to be due to the aging of male gametes within the female, and that at least some dead resident sperm remain in the female after multiple mating. In contrast to earlier in vivo work, we found that overall sperm death was minimal (8.7%), indicating viability should have a negligible influence on female remating rates.     

Adaptive speciation when assortative mating is based on female preference for male marker traits

Adaptive speciation occurs when frequency-dependent ecological interactions generate conditions of disruptive selection to which lineage splitting is an adaptive response. Under such selective conditions, evolution of assortative mating mechanisms enables the break-up of the ancestral lineage into diverging and reproductively isolated descendent species. Extending previous studies, I investigate models of adaptive speciation due to the evolution of indirect assortative mating that is based on three different mating traits: the degree of assortativity, a female preference trait and a male marker trait. For speciation to occur, linkage disequilibria between different mating traits, e.g. between female preference and male marker traits, as well as between mating traits and the ecological trait, must evolve. This can lead to novel speciation scenarios, e.g. when reproductive isolation is generated by a splitting in the degree of assortativeness, with one of the emerging lineages mating assortatively, and the other one disassortatively. I investigate the effects of variation in various model parameters on the likelihood of speciation, as well as robustness of speciation to introducing costs of assortative mating. Even though in the models presented speciation requires the genetic potential for strong assortment as well as rather restrictive ecological conditions, the results show that adaptive speciation due to the evolution of assortative mating when mate choice is based on separate female preference and male marker traits is a theoretically plausible evolutionary scenario.     

Enhanced cost of mating in female sterile mutants of Drosophila melanogaster

In Drosophila females, mating is known to cause a reduction in life span, which is referred to as 'the cost of mating'. Since mating enhances oogenesis and oviposition, the cost of mating may be regarded as a trade-off between reproduction and longevity. We examined whether the cost of mating exists in mutant females that are unable to produce eggs. Three different mutant alleles of ovarian tumors (otu) and an allele of dunce (dnc(M11)) of Drosophila melanogaster were used to sterilize females. For all the female sterile mutants tested, mating dramatically decreased the life span of homozygous sterile females. Even more extreme shortening of life spans were observed when the sex peptide gene (Acp70A) was expressed in homozygous otu females, though they were virgin, indicating that the shortening in life span is due to seminal factors. These results indicate that the cost of mating is greater in females defective in oogenesis than that in normally fertile females.     

Genetic analysis of female mating recognition between Drosophila ananassae and Drosophila pallidosa: application of interspecific mosaic genome lines

Drosophila ananassae and Drosophila pallidosa are closely related species that can produce viable and fertile hybrids of both sexes, although strong sexual isolation exists between the two species. Females are thought to discriminate conspecific from heterospecific males based on their courtship songs. The genetic basis of female discrimination behavior was analyzed using isogenic females from interspecific mosaic genome lines that carry homozygous recombinant chromosomes. Multiple regression analysis indicated a highly significant effect of the left arm of chromosome 2 (2L) on the willingness of females to mate with D. ananassae males. Not only 2L but also the left arm of chromosome X (XL) and the right arm of chromosome 3 (3R) had significant effects on the females' willingness to mate with D. pallidosa males. All regions with strong effects on mate choice have chromosome arrangements characterized by species-specific inversions. Heterospecific combinations of 2L and 3R have previously been suggested to cause postzygotic reproductive isolation. Thus, genes involved in premating as well as postmating isolation are located in or near chromosomal inversions. This conclusion is consistent with the recently proposed hypothesis that "speciation genes" accumulate at a higher rate in non-recombining genome regions when species divergence occurs in the presence of gene flow.     

The evolution of female mating preferences: differentiation from species with promiscuous males can promote speciation

Females of many species are frequently courted by promiscuous males of their own and other closely related species. Such mating interactions may impose strong selection on female mating preferences to favor trait values in conspecific males that allow females to discriminate them from their heterospecific rivals. We explore the consequences of such selection in models of the evolution of female mating preferences when females must interact with heterospecific males from which they are completely postreproductively isolated. Specifically, we allow the values of both the most preferred male trait and the tolerance of females for males that deviate from this most preferred trait to evolve. Also, we consider situations in which females base their mating decisions on multiple male traits and must interact with males of multiple species. Females will rapidly differentiate in preference when they sometimes mistake heterospecific males for suitable mates, and the differentiation of female preference will select for conspecific male traits to differentiate as well. In most circumstances, this differentiation continues indefinitely, but slows substantially once females are differentiated enough to make mistakes rare. Populations of females with broader preference functions (i.e., broader tolerance for males with trait values that deviate from females' most preferred values) will evolve further to differentiate if the shape of the function cannot evolve. Also, the magnitude of separation that evolves is larger and achieved faster when conspecific males have lower relative abundance. The direction of differentiation is also very sensitive to initial conditions if females base their mate choices on multiple male traits. We discuss how these selection pressures on female mate choice may lead to speciation by generating differentiation among populations of a progenitor species that experiences different assemblages of heterospecifics. Opportunities for differentiation increase as the number of traits involved in mate choice increase and as the number of species involved increases. We suggest that this mode of speciation may have been particularly prevalent in response to the cycles of climatic change throughout the Quaternary that forced the assembly and disassembly of entire communities on a continentwide basis.     

日本食蚧蚜小蜂的交配行为及雌蜂生殖系统观察

日本食蚧蚜小蜂Coccophagus japonicus Compere是橡副珠蜡蚧Parasaissetia nigra Nietner的优势寄生蜂之一,为明确其交配行为及雌蜂生殖系统构成,本研究在室内观察了该蜂的交配行为、雄蜂交配能力、雌蜂生殖系统等。结果表明:日本食蚧蚜小蜂的交配过程可分为交配前行为、交配、交配后行为3个阶段,整个交配过程平均时间为76.2 s,其中,交配时间为20.6 s;小蜂羽化当天即可交配,雌、雄蜂具有多次交配的习性,雄蜂的交配能力随其日龄的增加而减弱,1日龄的雄蜂交配能力最强,为6.3次/d,雄蜂一生平均能交配36.9次;雌蜂的生殖系统由1对卵巢、1对侧输卵管、1条中输卵管、1个受精囊和外生殖器等组成,卵巢管数量存在变异,其中95.78%雌蜂卵巢具6(3+3)条卵巢管,2.78%雌蜂卵巢具5(3+2)条卵巢管,1.22%的雌蜂卵巢具7(3+4)条卵巢管,0.22%的雌蜂卵巢是具4(2+2,1+3)条卵巢管,还有极个别的雌蜂仅有1个卵巢,由3条卵巢管组成。研究结果表明日本食蚧蚜小蜂有多次交配习性,卵巢存在一定变异。     

Facultative pupal mating in Heliconius erato: Implications for mate choice,female preference,and speciation

Mating systems have broad impacts on how sexual selection and mate choice operate within a species, but studies of mating behavior in the laboratory may not reflect how these processes occur in the wild. Here, we examined the mating behavior of the neotropical butterfly Heliconius erato in the field by releasing larvae and virgin females and observing how they mated. H. erato is considered a pupal‐mating species (i.e., males mate with females as they emerge from the pupal case). However, we observed only two teneral mating events, and experimentally released virgins were almost all mated upon recapture. Our study confirms the presence of some pupal‐mating behavior in H. erato, but suggests that adult mating is likely the prevalent mating strategy in this species. These findings have important implications for the role of color pattern and female mate choice in the generation of reproductive isolation in this diverse genus.     

Endocrinology of human female sexuality,mating, and reproductive behavior

Hormones orchestrate and coordinate human female sexual development, sexuality, and reproduction in relation to three types of phenotypic changes: life history transitions such as puberty and childbirth, responses to contextual factors such as caloric intake and stress, and cyclical patterns such as the ovulatory cycle. Here, we review the endocrinology underlying women's reproductive phenotypes, including sexual orientation and gender identity, mate preferences, competition for mates, sex drive, and maternal behavior. We highlight distinctive aspects of women's sexuality such as the possession of sexual ornaments, relatively cryptic fertile windows, extended sexual behavior across the ovulatory cycle, and a period of midlife reproductive senescence—and we focus on how hormonal mechanisms were shaped by selection to produce adaptive outcomes. We conclude with suggestions for future research to elucidate how hormonal mechanisms subserve women's reproductive phenotypes.     

Rhythmicity of sex pheromone content in female Heliothis virescens: impact of mating

Abstract Pheromone production in virgin females of Heliothis virescens (F.) (Lepidoptera: Noctuidae) peaked between the fourth and seventh hours of scotophase on the second, third, fourth and fifth days following eclosion. The highest peak (186 ng) occurred on day 3 after eclosion. Z-11-Hexadecenal comprised the highest proportion of seven components in the pheromone glands. Disproportionately higher amounts of hexadecanal and Z-11-hexadecenol occurred during photo-phase and other periods when low quantities of total pheromone were recorded.
Mating suppressed pheromone production which remained low until 48 h after mating. Coupling females with males mated three times previously or with 6-day-old males was less effective in causing a drop in pheromone content which peaked again 24 h after mating. This suggests the transfer of a male factor, a pheromonostatic factor, that suppresses pheromone production in mated females and that the factor from older and previously mated males is less effective.