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A possible non-sexual origin of mate preference: are male guppies mimicking fruit?

In most animals, the origins of mating preferences are not clear. The "sensory-bias" hypothesis proposes that biases in female sensory or neural systems are important in triggering sexual selection and in determining which male traits will become elaborated into sexual ornaments. Subsequently, other mechanisms can evolve for discriminating between high- and low-quality mates. Female guppies (Poecilia reticulata) generally show a preference for males with larger, more chromatic orange spots. It has been proposed that this preference originated because it enabled females to obtain high-quality mates. We present evidence for an alternative hypothesis, that the origin of the preference is a pleiotropic effect of a sensory bias for the colour orange, which might have arisen in the context of food detection. In field and laboratory experiments, adult guppies of both sexes were more responsive to orange-coloured objects than to objects of other colours, even outside a mating context. Across populations, variation in attraction to orange objects explained 94% of the inter-population variation in female mate preference for orange coloration on males. This is one of the first studies to show both an association between a potential trigger of a mate-choice preference and a sexually selected trait, and also that an innate attraction to a coloured inanimate object explains almost all of the observed variation in female mate choice. These results support the "sensory-bias" hypothesis for the evolution of mating preferences.

Animals↗

A demographic analysis of the components of selection in a population of Arctic Skuas.

From previously published demographic data of the age distributions and reproductive rates of the pale, intermediate and dark phenotypes of the Arctic Skua, revised estimates are obtained of the intrinsic rates of increase and selective coefficients of the phenotypes in each sex. Two significant components of selection are variation in age of maturity and variation in reproductive success. Sexual selection is a component of the variation in reproductive success. Dark and intermediate birds have a greater reproductive success than pales, partly as a result of their advantage in sexual selection. Pale birds have an overall advantage, however, because they are younger when they first breed. Given the estimated selective coefficients, a computer model predicts that pale birds will gradually replace the others. So far there are not enough data collected over a sufficiently long time to test the model rigorously.

Animals↗

Effect of larval crowding on adult mating behaviour in Drosophila melanogaster.

The effect of larval density on male mating success has been investigated with two strains of Drosophila melanogaster, a wild strain and a mutant strain, under low and high larval competition, and four different genotypic frequencies. The results show a strong sexual selection against mutant males when flies have been raised under low larval competition. Under high larval competition, there is a reduction in mating disadvantage of mutant males. In both instances, a frequency-dependent sexual selection exists. These results explain adequately the evolution of experimental populations where egg to adult viability and male mating success are the most important components of fitness.

Alleles↗

Climatic and temporal effects on the expression of secondary sexual characters: genetic and environmental components.

Despite great interest in sexual selection, relatively little is known in detail about the genetic and environmental determinants of secondary sexual characters in natural populations. Such information is important for determining the way in which populations may respond to sexual selection. We report analyses of genetic and large-scale environmental components of phenotypic variation of two secondary sexual plumage characters (forehead and wing patch size) in the collared flycatcher Ficedula albicollis over a 22-year period. We found significant heritability for both characters but little genetic covariance between the two. We found a positive association between forehead patch size and a large-scale climatic index, the North Atlantic Oscillation (NAO) index, but not for wing patch. This pattern was observed in both cross-sectional and longitudinal data suggesting that the population response to NAO index can be explained as the result of phenotypic plasticity. Heritability of forehead patch size for old males, calculated under favorable conditions (NAO index > or = median), was greater than that under unfavorable conditions (NAO index < median). These changes occurred because there were opposing changes in additive genetic variance (VA) and residual variance (VR) under favorable and unfavorable conditions, with VA increasing and VR decreasing in good environments. However, no such effect was detected for young birds, or for wing patch size in either age class. In addition to these environmental effects on both phenotypic and genetic variances, we found evidence for a significant decrease of forehead patch size over time in older birds. This change appears to be caused by a change in the sign of viability selection on forehead patch size, which is associated with a decline in the breeding value of multiple breeders. Our data thus reveal complex patterns of environmental influence on the expression of secondary sexual characters, which may have important implications for understanding selection and evolution of these characters.

Age Factors↗

Male-female conflict and genitalia: failure to confirm predictions in insects and spiders.

Some recent models suggest a new role for evolutionary arms races between males and females in sexual selection. Female resistance to males is proposed to be driven by the direct advantage to the female of avoiding male-imposed reductions in the number of offspring she can produce, rather than by the indirect advantage of selecting among possible sires for her offspring, as in some traditional models of sexual selection by female choice. This article uses the massive but hitherto under-utilized taxonomic literature on genitalic evolution to test, in a two-step process, whether such new models of arms races between males and females have been responsible for rapid divergent evolution of male genitalia. The test revolves around the prediction that 'new arms races' are less likely to occur in species in which females are largely or completely protected from unwanted sexual attentions from males (e.g. species which mate in leks or in male swarms, in which males attract females from a distance, or in which females initiate contact by attracting males from a distance). The multiple possible mechanical functions of male genitalia are summarized, and functions of male genitalic structures in 43 species in 21 families of Diptera are compiled. Functions associated with intromission and insemination (e.g. seizing and positioning the female appropriately, pushing past possible barriers within the female, orienting within the female to achieve sperm transfer), which are unlikely to be involved in new arms races when females are protected, are shown to be common (> 50 % of documented cases). This information is then used to generate the new arms race prediction: differences in genitalic form among congeneric species in which females are protected should be less common than differences among congeneric species in which females are vulnerable to harassment by males. This prediction was tested using a sample of 361 genera of insects and spiders. The prediction clearly failed, even when the data were adjusted to take into account several possible biases. Comparative analyses within particular taxonomic groups also failed to show the predicted trends, as did less extensive data on other non-genitalic male display traits. Arms races, as defined in some recent models, seem to have been less important in male-female coevolution of genitalic structures than has been suggested. By elimination, alternative interpretations, such as traditional female choice, which do not predict associations between female protection from harassment and rapid divergent evolution, are strengthened.

Animals↗

Sexual isolation among widely distributed populations of Drosophila immigrans.

Six strains of the cosmopolitan species D. immigrans from the Australian life zone plus one from the USA, show weak sexual isolation and more rarely sexual selection. Levels of sexual isolation cannot be related to geographic distances. Assortative mating may have evolved as a byproduct of ecological divergence.

Animals↗

The biology and evolution of music: a comparative perspective.

Studies of the biology of music (as of language) are highly interdisciplinary and demand the integration of diverse strands of evidence. In this paper, I present a comparative perspective on the biology and evolution of music, stressing the value of comparisons both with human language, and with those animal communication systems traditionally termed "song". A comparison of the "design features" of music with those of language reveals substantial overlap, along with some important differences. Most of these differences appear to stem from semantic, rather than structural, factors, suggesting a shared formal core of music and language. I next review various animal communication systems that appear related to human music, either by analogy (bird and whale "song") or potential homology (great ape bimanual drumming). A crucial comparative distinction is between learned, complex signals (like language, music and birdsong) and unlearned signals (like laughter, ape calls, or bird calls). While human vocalizations clearly build upon an acoustic and emotional foundation shared with other primates and mammals, vocal learning has evolved independently in our species since our divergence with chimpanzees. The convergent evolution of vocal learning in other species offers a powerful window into psychological and neural constraints influencing the evolution of complex signaling systems (including both song and speech), while ape drumming presents a fascinating potential homology with human instrumental music. I next discuss the archeological data relevant to music evolution, concluding on the basis of prehistoric bone flutes that instrumental music is at least 40,000 years old, and perhaps much older. I end with a brief review of adaptive functions proposed for music, concluding that no one selective force (e.g., sexual selection) is adequate to explaining all aspects of human music. I suggest that questions about the past function of music are unlikely to be answered definitively and are thus a poor choice as a research focus for biomusicology. In contrast, a comparative approach to music promises rich dividends for our future understanding of the biology and evolution of music.

Animal Communication↗

Early determinants of lifetime reproductive success differ between the sexes in red deer.

In polygynous, sexually dimorphic species, sexual selection should be stronger in males than in females. Although this prediction extends to the effects of early development on fitness, few studies have documented early determinants of lifetime reproductive success in a natural mammal population. In this paper, we describe factors affecting the reproductive success of male and female red deer (Cervus elaphus) on the island of Rum, Scotland. Birthweight was a significant determinant of total lifetime reproductive success in males, with heavier-born males being more successful than lighter ones. In contrast, birthweight did not affect female reproductive success. High population density and cold spring temperatures in the year of birth decreased several components of fitness in females, but did not affect the breeding success of males. The results confirm the prediction that selection on a sexually dimorphic trait should be greater in males than in females, and explain the differential maternal expenditure between sons and daughters observed in red deer. Differences between the sexes in the effects of environmental and phenotypic variation on fitness may generate differences in the amount of heritable genetic variation underlying traits such as birthweight.

Adaptation, Physiological↗

Age-dependent sexually asymmetric selection: the use of intrinsic values.

To study the evolutionary role played by differential male and female fertility (sexual asymmetry) both between individuals and over the life span within single individuals, the terms "intrinsic male fertility" and "intrinsic female fertility" are introduced. With the help of these terms, the concept of sexual asymmetry can be made precise and its effect on the establishment and maintenance of genetic polymorphisms can be analyzed. The main conclusions are: (1) any mutant causing a modification of the male fertility parameters which result in an increased intrinsic male fertility becomes established; (2) a corollary of this is that age-specific sexual asymmetry, as results from alternating degrees of female and male flowering in successive reproduction cycles, for example, has only secondary effects on the initial growth rate; (3) under the biologically reasonable premise that modifications of life histories result from reallocation of fixed net reproduction resources (defined as constant total female and male net reproduction output), a shift of net reproduction (whether female, male, or both in arbitrary proportions) to earlier ages is evolutionarily successful in growing but not in declining populations; shifts of net reproduction to later ages have opposite consequences.

Age Factors↗

Carotenoid Plasma Concentration, Immune Profile, and Plumage Ornamentation of Male Barn Swallows (Hirundo rustica).

Carotenoids exert immunomodulating, immunostimulating, and antioxidant actions in mammals and are major determinants of coloration in animals. Honest advertisement models of sexual selection propose that male ornaments, including coloration, are reliable indicators of male quality. Because of their simultaneous effects on male coloration and immunity, carotenoids might mediate the hypothesized relationship between the expression of epigamic coloration and parasitism in vertebrates. We analyzed the relationship between immune profile and concentration of lutein, the most abundant carotenoid in the plasma of male barn swallows (Hirundo rustica). Consistent with our predictions, lutein plasma concentration was negatively correlated with gamma-globulin plasma levels and concentration of selected leukocyte types in peripheral blood, suggesting that, to exert immune function, carotenoids are taken up from plasma, thus becoming unavailable for epigamic signaling. The coloration of red feathers of the throat of adult males was positively related to plasma concentration of lutein, but not with immunologic variables, consistent with the idea that more brightly colored males do not pay a larger immunological cost for their coloration compared with less brightly colored males. Length of male tail ornaments, which is currently under directional sexual selection, was positively correlated with lutein plasma levels. In species where carotenoids limit immune function, demands for pigments for sexual signaling might compete with those for immunity, thus generating a mechanism that enforces honesty on the signal.

immunity↗

Evolution of exclusive paternal care in arthopods.

Exclusive male care of offspring is the rarest form of postzygotic parental care among animals and has arisen independently in only 13 arthropod taxa. To distinguish the effects of sexual selection from those of natural selection on the evolution of arthropod paternal care, predictions concerning several life-history and behavioral traits resulting from both forms of selection are made and tested across all known taxa with exclusive paternal care. Comparisons suggest parallels between prezygotic nuptial gifts and exclusive postzygotic male care and support the hypothesis that, in arthropods, male behaviors that enhance female reproductive success either directly, by releasing females from the fecundity constraints of maternal care (enhanced fecundity hypothesis), or indirectly, by identifying mates with superior genes (handicap principle), are traits on which sexual selection has acted. Under such conditions, males that are willing to guard young become preferred mates for gravid females and enjoy greater promiscuity than males that are unable or unwilling to guard. Females use nest construction or the act of guarding another female's eggs as honest signals of paternal intent and quality.

Animals↗

Sexual dimorphism in primate evolution.

Sexual dimorphism is a pervasive phenomenon among anthropoid primates. Comparative analyses over the past 30 years have greatly expanded our understanding of both variation in the expression of dimorphism among primates, and the underlying causes of sexual dimorphism. Dimorphism in body mass and canine tooth size is familiar, as is pelage and "sex skin" dimorphism. More recent analyses are documenting subtle differences in the pattern of skeletal dimorphism among primates. Comparative analyses have corroborated the sexual selection hypotheses, and have provided a more detailed understanding of the relationship between sexual selection, natural selection, and mating systems in primates. A clearer picture is emerging of the relative contribution of various selective and nonselective mechanisms in the evolution and expression of dimorphism. Most importantly, recent studies have shown that dimorphism is the product of changes in both male and female traits. Developmental studies demonstrate the variety of ontogenetic pathways that can lead to dimorphism, and provide additional insight into the selective mechanisms that influence dimorphism throughout the lifetime of an animal. Evidence from the fossil record suggests that dimorphism probably evolved in parallel twice, and the dimorphism in some extinct hominoids probably exceeded that of any living primate. Our advances in understanding the behavioral/ecological correlates of dimorphism in living primates have not improved our ability to reconstruct social systems in extinct species on the basis of dimorphism alone, beyond the inference of polygyny or intense male-male competition. However, our understanding of the behavioral/ecological correlates of growth and development, and of the expression of dimorphism as a function of separate changes in male and female traits, offers great potential for inferring evolutionary changes in behavior over time.

Animals↗

Opposing selection on a sexually dimorphic trait through female choice and male competition in a water boatman.

Female choice and male-male competition are traditionally considered to act in concert, with male competition facilitating female choice. This situation would enforce the strength of directional selection, which could reduce genetic variation and thus the benefits of choice. Here I show that in a water boatman, Sigara falleni, the direction of selection through female choice and male competition vary among traits under laboratory conditions. The two forces were mutually enforcive in acting on body size but exerted opposing selection on a sexually selected trait, male foreleg pala size. Female choice favored large palae, whereas male competition favored smaller palae, suggesting that large palae are costly in competition. This conflicting selection through female choice and male competition could be one of the forces that contribute to the maintenance of genetic variation in sexually selected traits.

Animals↗

Sex-specific spawning behavior and its consequences in an external fertilizer.

Identifying the target of sexual selection in externally fertilizing taxa has been problematic because species in these taxa often lack sexual dimorphism. However, these species often show sex differences in spawning behavior; males spawn before females. I investigated the consequences of spawning order and time intervals between male and female spawning in two field experiments. The first involved releasing one female sea urchin's eggs and one or two males' sperm in discrete puffs from syringes; the second involved inducing males to spawn at different intervals in situ within a population of spawning females. In both, fertilization success was measured as the fraction of eggs fertilized and the paternity share of each male. The results indicate that spawning after females imposes a cost on males but only during sperm competition. Further, the optimal interval between the initiations of male and female spawning depends on degree of sperm competition, distance between males and females, and water velocity. The results show that sex differences in spawning timing of marine invertebrates can be explained on the basis of the differential costs and benefits of spawning out of synchrony with the other sex and that the result of sexual selection on external fertilizers may be behavioral rather than morphological differentiation of the sexes.

Animals↗

Positive genetic correlation between female preference and offspring fitness.

In many species, females display preferences for extreme male signal traits, but it has not been determined if such preferences evolve as a consequence of females gaining genetic benefits from exercising choice. If females prefer extreme male traits because they indicate male genetic quality that will enhance the fitness of offspring, a genetic correlation will evolve between female preference genes and genes that confer offspring fitness. We show that females of Drosophila serrata prefer extreme male cuticular hydrocarbon (CHC) blends, and that this preference affects offspring fitness. Female preference is positively genetically correlated with offspring fitness, indicating that females have gained genetic benefits from their choice of males. Despite male CHCs experiencing strong sexual selection, the genes underlying attractive CHCs also conferred lower offspring fitness, suggesting a balance between sexual selection and natural selection may have been reached in this population.

Animals↗

Evolutionary experiments on mate recognition in the Drosophila serrata species complex.

It is becoming increasingly apparent that at least some aspects of the evolution of mate recognition may be amenable to manipulation in evolutionary experiments. Quantitative genetic analyses that focus on the genetic consequences of evolutionary processes that result in mate recognition evolution may eventually provide an understanding of the genetic basis of the process of speciation. We review a series of experiments that have attempted to determine the genetic basis of the response to natural and sexual selection on mate recognition in the Drosophila serrata species complex. The genetic basis of mate recognition has been investigated at three levels: (1) between the species of D. serrata and D. birchii using interspecific hybrids, (2) between populations of D. serrata that are sympatric and allopatric with respect to D. birchii, and (3) within populations of D. serrata. These experiments suggest that it may be possible to use evolutionary experiments to observe important events such as the reinforcement of mate recognition, or the generation of the genetic associations that are central to many sexual selection models.

Animals↗

Male sex drive and the masculinization of the genome.

Charles Darwin remarked that "males, with their superior strength, pugnacity, armaments, unwieldly passion and love songs, are almost always the more active and most often, the initiators of sexual interactions". Here, we propose that such male sex drive directly impacts the genome by leading to its progressive masculinization--genes that possess sex-specific effects on male fitness accumulate to a much greater extent and are generally more diverged. The larger proportion of male versus female fitness modifiers in combination with stronger sexual selection may generate evolutionary signatures such as a greater sensitivity to male sterility and a paucity of X-linked male-specific genes. Male sex-drive theory complements the female-choice theory of sexual selection and allows for the genetic variation of costly sexual traits to be continuously replenished.

Animals↗

Increased sexual activity reduces male immune function in Drosophila melanogaster.

Despite the benefits of resistance, susceptibility to infectious disease is commonplace. Although specific susceptibility may be considered an inevitable consequence of the co-evolutionary arms race between parasite and host, a more general constraint may arise from the cost of an immune response. This "cost" hypothesis predicts a tradeoff between immune defense and other components of fitness. In particular, a tradeoff between immunity and sexually selected male behavior has been proposed. Here we provide experimental support for the direct phenotypic tradeoff between sexual activity and immunity by studying the antibacterial immune response in Drosophila melanogaster. Males exposed to more females showed a reduced ability to clear a bacterial infection, an effect that we experimentally link to changes in sexual activity. Our results suggest immunosuppression is an important cost of reproduction and that immune function and levels of disease susceptibility will be influenced by sexual selection.

Animals↗