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Female preference for conspecific males based on olfactory cues in a Lake Malawi cichlid fish.

Research on reproductive isolation in African cichlid fishes has largely focused on the role of nuptial colours, but other sensory modes may play an important role in mate choice. Here, we compare the relative importance of visual and olfactory cues in mate recognition by females of a Lake Malawi cichlid species. Female Pseudotropheus emmiltos were given a choice of spawning next to a conspecific male or a male of the closely-related sympatric Pseudotropheus fainzilberi. Significant preference for conspecific males only occurred when olfactory cues were present. This suggests that divergence of olfactory signals may have been an important influence on the explosive radiation of the East African species flock.

Animals↗

Polymorphisms in the HLA-linked olfactory receptor genes in the Hutterites.

Genes in the MHC have been associated with mate choice and odor preferences in a variety of animals. Although the role of HLA genes in human mate choice has been controversial, studies in the Hutterites have demonstrated fewer than expected numbers of couples who match for an HLA haplotype, suggesting that in this population there is avoidance of mates with HLA haplotypes similar to one's own haplotype. Recently, 18 olfactory receptor (OR) genes have been mapped to the HLA region, telomeric to the HLA-F locus, providing a potential mechanism for HLA-based odor recognition and perhaps mate preferences in humans. We screened a sample of Hutterites with diverse HLA haplotypes for polymorphisms in the HLA-linked olfactory receptor gene, FAT11, by sequencing, denaturing high performance liquid chromatography, and allele-specific oligo dot-blotting. Three single nucleotide polymorphisms were detected in the single translated exon of this gene, all of which resulted in amino acid substitutions (Phe587Leu, Ala642Val, and Thr1157Ala). The FAT11 Phe587- Val642-Ala1157 allele occurred on 17 different HLA haplotypes, the Leu587-Ala642-Ala1157 allele on 15 haplotypes, the Phe587-Ala642-Ala1157 allele on 16 haplotypes, and the Phe587-Ala642-Thr1157 allele on a single haplotype. Thus, four alleles of the FAT11 gene are present in the Hutterites. This level of variation in the FAT11 gene alone may not be sufficient to contribute to the observed patterns of mate choice in the Hutterites and to individual variation in odor preferences.

Alleles↗

Sexual imprinting can induce sexual preferences for exaggerated parental traits.

Sexual preferences in animals are often skewed toward mates with exaggerated traits. In many vertebrates, parents provide, through the learning process of "sexual imprinting," the model for the later sexual preference. How imprinting can result in sexual preferences for mates having exaggerated traits rather than resembling the parental appearance is not clear. We test the hypothesis that a by-product of the learning process, "peak shift", may induce skewed sexual preferences for exaggerated parental phenotypes. To this end, zebra finch (Taeniopygia guttata) males were raised by white parents, with beak color as the most prominent sexual dimorphism. We manipulated this feature with nail varnish. At adult age, each male was given a preference test in which he could choose among eight females with beak colors ranging from more extreme on the paternal to more extreme on the maternal side. The males preferred females with a beak of a more extreme color than that of their mothers, i.e., they showed a peak shift. Sexual imprinting can thus generate skewed sexual preferences for exaggerated maternal phenotypes, phenotypes that have not been present at the time of the learning. We suggest that such preferences can drive the evolution of sexual dimorphism and exaggerated sexual traits.

Animals↗

Sensory drive in cichlid speciation.

The role of selection in speciation is a central yet poorly understood problem in evolutionary biology. The rapid radiations of extremely colorful cichlid fish in African lakes have fueled the hypothesis that sexual selection can drive species divergence without geographical isolation. Here we present experimental evidence for a mechanism by which sexual selection becomes divergent: in two sibling species from Lake Victoria, female mating preferences for red and blue male nuptial coloration coincide with their context-independent sensitivities to red and blue light, which in turn correspond to a difference in ambient light in the natural habitat of the species. These results suggest that natural selection on visual performance, favoring different visual properties in different spectral environments, may lead to divergent sexual selection on male nuptial coloration. This interplay of ecological and sexual selection along a light gradient may provide a mechanism of rapid speciation through divergent sensory drive.

Adaptation, Biological↗

Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless.

Sexual isolation is a critical form of reproductive isolation in the early stages of animal speciation, yet little is known about the genetic basis of divergent mate preferences and preference cues in young species. Heliconius butterflies, well known for their diversity of wing color patterns, mate assortatively as a result of divergence in male preference for wing patterns. Here we show that the specific cue used by Heliconius cydno and Heliconius pachinus males to recognize conspecific females is the color of patches on the wings. In addition, male mate preference segregates with forewing color in hybrids, indicating a genetic association between the loci responsible for preference and preference cue. Quantitative trait locus mapping places a preference locus coincident with the locus that determines forewing color, which itself is perfectly linked to the wing patterning candidate gene, wingless. Furthermore, yellow-colored males of the polymorphic race H. cydno alithea prefer to court yellow females, indicating that wing color and color preference are controlled by loci that are located in an inversion or are pleiotropic effects of a single locus. Tight genetic associations between preference and preference cue, although rare, make divergence and speciation particularly likely because the effects of natural and sexual selection on one trait are transferred to the other, leading to the coordinated evolution of mate recognition. This effect of linkage on divergence is especially important in Heliconius because differentiation of wing color patterns in the genus has been driven and maintained by natural selection for Müllerian mimicry.

Animals↗

Sexual selection with a culturally transmitted mating preference.

Culturally transmitted mating preferences may generate sexual selection in human and protocultural animal species if they influence the intensity of selection on genetically transmitted physical and behavioral traits. Haploid and diploid two-"locus" models of sexual selection are presented in which mating preferences are culturally transmitted, while traits are transmitted genetically. The models exhibit dynamics similar to those of conventional haploid models of sexual selection, generating neutrally stable curves of equilibrium trait and preference frequencies. A culturally transmitted preference that reaches a significant frequency through cultural drift, individual learning, or social transmission can drag a less viable trait to fixation, or non-zero frequencies. Simulations suggest that strong biases in the transmission of preferences could take initially rare, less viable traits to fixation in as few as 20 to 50 generations, and weak biases in less than 100 generations. These conclusions hold for both biparental and maternally inherited mating preferences. Given the pervasiveness of cultural influences on human mate choice, the analysis suggests that this interaction may have played an important role in human evolution.

Animals↗

Sensory neurons with MHC-like peptide binding properties: disease consequences.

The recent discovery of specialized sensory neurons that bind peptides in an MHC-like fashion has revealed the long-sought odorants used to recognize the MHC genotype and phenotype of other individuals. The odorants are the same MHC peptides used during immune recognition, which provides the molecular logic linking selection acting on MHC-mediated behaviors with selection acting on immune recognition; both processes influence the evolving peptide binding properties of MHC molecules. The primary function of these chemosensory mechanisms for detecting MHC-mediated odors appears to be mating preferences (observed in humans and many vertebrates) that preferentially produce offspring more resistant to both infectious and genetic disease. Recent experiments are beginning to discriminate the relative importance of these different disease-reducing mechanisms.

Animals↗

Extensive MHC class II DRB3 diversity in African and European cattle.

Genetic diversity at the highly polymorphic BoLA-DRB3 locus was investigated by DNA sequence analyses of 18 African cattle from two breeds representing the two subspecies of cattle, Bos primigenius indicus and Bos primigenius taurus. The polymorphism was compared with that found in a sample of 32 European cattle from four breeds, all classified as B. p. taurus. Particularly extensive genetic diversity was found among African cattle, in which as many as 18 alleles were recognized in this small random sample of animals from two breeds. The observed similarity in allele frequency distribution between the two African populations, N'Dama and Zebu cattle, is consistent with the recent recognition of gene flow between B. p. indicus and B. p. taurus cattle in Africa. A total of 30 DRB3 alleles were documented and as many as 26 of these were classified as major allelic types showing at least five amino acid substitutions compared with other major types. The observation of extensive genetic diversity at MHC loci in cattle, as well as in other farm animals, provides a compelling argument against mating-type preferences as a primary cause in maintaining major histocompatibility complex diversity, since the reproduction of these animals has been controlled by humans for many generations.

Africa↗

Fisherian and Wrightian theories of speciation.

Fisher's theory of sexual selection, Wright's shifting-balance theory, and recent models based on them are reviewed as mechanisms of animal speciation. The joint evolution of mating preferences and secondary sexual characters can cause rapid nonadaptive phenotypic divergence and premating isolation between geographically separated populations, or along a cline. Extensive comparative data on Drosophila species support the suggestion of R. A. Fisher and T. Dobzhansky that the evolution of mating preferences can reinforce partial postmating isolation between sympatric populations. The interaction of natural selection and random genetic drift in local populations with a small effective size can produce a rapid transition between relatively stable phenotypes separated by an adaptive valley, or between chromosomal rearrangements with a heterozygote disadvantage. Large demographic fluctuations, such as frequent random local extinction and colonization, are required for the rapid spread of new adaptations (or karyotypes) when intermediate phenotypes (or rearrangement heterozygotes) are selected against.

Animals↗

Mating in the monogamous male: behavioral consequences.

In monogamous mammals, males typically show selective affiliation with a single mate, high levels of paternal care, and aggression towards conspecifics to protect male and offspring. We have previously described how selective aggression and affiliation increase after mating in the male prairie vole, Microtus ochrogaster. The current studies further explored the behavioral changes that follow mating in the male of this species. The first set of experiments tested males on several behavioral measures after 24 h of either mating, social (but not sexual) exposure, or no social contact. After 24 h of mating, but not after the other two conditions, aggression and affiliation (partner preference) increased as previously reported. In addition, mated animals showed increased exploration of the open arms of a plus maze, consistent with decreased fearfulness. There were no group differences in paternal behavior (which was high in all three conditions) or analgesia (assessed by tail flick latency). To determine the minimum amount of mating necessary for the induction of aggression, males were tested in a resident-intruder paradigm after 1,6, or 24 h of mating. Although 1 h of mating was associated with a transient increase in the frequency of threats and attacks, the full spectrum of enduring aggression was observed only in the males given 24 h of mating. In a final experiment, the behavioral consequences of mating were studied in males of the closely related montane vole (Microtus montanus) which does not pair bond. Males of this nonmonogamous vole species did not show increased aggression, partner preference, or alterations in plus maze exploration following 24 h of mating. These results demonstrate the importance of prolonged mating for the induction of pair bonding in the monogamous male and they suggest that increases in aggression and affiliation are associated with decreased fearfulness in pair bonded males.

Aggression↗

Mode of mating preference and the direction of evolution in Drosophila.

Sexual (or ethological) isolation constitutes the most important class among different means of reproductive isolation in animal species. The phenomenon of sexual isolation has been extensively studied in the genus Drosophila. The degree of sexual isolation and the mode of mating preference are often used to indicate the phylogenetic relationship between the species and also their evolutionary sequence. Asymmetrical or one-sided mating preference observed in a number of Drosophila species groups has been used to elucidate the direction of evolution. Based on the mode of mating preference, different models which are even opposite to each other have been proposed by different investigators to predict the direction of evolution among closely related species. One-sided mating preference observed among the geographical strains of the same species has also been used to predict the direction of evolution. This review documents several cases of asymmetrical mating preference (both inter- and intraspecific) including the interesting cases reported by Indian workers and in the light of these observations of asymmetry in mating preference, the general applicability of different models is discussed.

Animals↗

Mating advantage of rare males in models of sexual selection.

Models of sexual selection in polygynous species of animals have been derived on the assumption that some females have preferences to mate with males with particular genotypes. The mating advantage gained by the males is always frequency-dependent because the preferred males take part in the same number of preferential matings when they are rare as when they are common; individually therefore, they mate more often when they are rare. Frequency-dependent sexual selection has been demonstrated in many experiments with Drosophila: rare males take part in a higher proportion of matings than their frequency as available mates. Ehrman and Spiess explained this phenomenon by frequency-dependence either in female preference or in male courtship. This explanation, which is difficult to interpret in behavioural terms, may not be necessary, however, because constant female preferences would entail frequency-dependent selection among the males. I show here that a simple model of constant preferences for particular phenotypes or genotypes is sufficient to explain a large body of data on frequency-dependent sexual selection in Drosophila.

Alleles↗

MHC-dependent mate preferences in humans.

One substantial benefit of sexual reproduction could be that it allows animals (including humans) to react rapidly to a continuously changing environmental selection pressure such as coevolving parasites. This counteraction would be most efficient if the females were able to provide their progeny with certain allele combinations for loci which may be crucial in the parasite-host arms race, for example the MHC (major histocompatibility complex). Here we show that the MHC influences both body odours and body odour preferences in humans, and that the women's preferences depend on their hormonal status. Female and male students were typed for their HLA-A, -B and -DR. Each male student wore a T-shirt for two consecutive nights. The next day, each female student was asked to rate the odours of six T-shirts. They scored male body odours as more pleasant when they differed from the men in their MHC than when they were more similar. This difference in odour assessment was reversed when the women rating the odours were taking oral contraceptives. Furthermore, the odours of MHC-dissimilar men remind the test women more often of their own actual or former mates than do the odours of MHC-similar men. This suggests that the MHC or linked genes influence human mate choice today.

Adult↗