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The evolution of beauty : how Darwin's forgotten theory of mate choice shapes the animal world -- and us
What can explain the incredible diversity of beauty in nature? Richard O. Prum, an award-winning ornithologist, discusses Charles Darwin's second and long-neglected theory--aesthetic mate choice--and what it means for our understanding of evolution. In addition, Prum connects those same evolutionary dynamics to the origins and diversity of human sexuality, offering riveting new thinking about the evolution of human beauty and the role of mate choice, thereby transforming our ancestors from typical infanticidal primates into socially intelligent, pair-bonding caregivers. Prum's book is an exhilarating tour de force that begins in the trees and ends by fundamentally challenging how we understand human evolution and ourselves. -- adapted from dust jacket.
Book
Assortative Mating in Animals
Assortative mating occurs when there is a correlation (positive or negative) between male and female phenotypes or genotypes across mated pairs. To determine the typical strength and direction of assortative mating in animals, we carried out a meta-analysis of published measures of assortative mating for a variety of phenotypic and genotypic traits in a diverse set of animal taxa. We focused on the strength of assortment within populations, excluding reproductively isolated populations and species. We collected 1,116 published correlations between mated pairs from 254 species (360 unique species-trait combinations) in five phyla. The mean correlation between mates was 0.28, showing an overall tendency toward positive assortative mating within populations. Although 19% of the correlations were negative, simulations suggest that these could represent type I error and that negative assortative mating may be rare. We also find significant differences in the strength of assortment among major taxonomic groups and among trait categories. We discuss various possible reasons for the evolution of assortative mating and its implications for speciation.
Journal Article
Mechanisms of Assortative Mating in Speciation with Gene Flow
The large body of theory on speciation with gene flow has brought to light fundamental differences in the effects of two types of mating rules on speciation: preference/trait rules, in which divergence in both (female) preferences and (male) mating traits is necessary for assortment, and matching rules, in which individuals mate with like individuals on the basis of the presence of traits or alleles that they have in common. These rules can emerge from a variety of behavioral or other mechanisms in ways that are not always obvious. We discuss the theoretical properties of both types of rules and explain why speciation is generally thought to be more likely under matching rather than preference/trait rules. We furthermore discuss whether specific assortative mating mechanisms fall under a preference/trait or matching rule, present empirical evidence for these mechanisms, and propose empirical tests that could distinguish between them. The synthesis of the theoretical literature on these assortative mating rules with empirical studies of the mechanisms by which they act can provide important insights into the occurrence of speciation with gene flow. Finally, by providing a clear framework we hope to inspire greater alignment in the ways that both theoreticians and empiricists study mating rules and how these rules affect speciation through maintaining or eroding barriers to gene flow among closely related species or populations.
Journal Article
The scale-of-choice effect and how estimates of assortative mating in the wild can be biased due to heterogeneous samples
The mode in which sexual organisms choose mates is a key evolutionary process, as it can have a profound impact on fitness and speciation. One way to study mate choice in the wild is by measuring trait correlation between mates. Positive assortative mating is inferred when individuals of a mating pair display traits that are more similar than those expected under random mating while negative assortative mating is the opposite. A recent review of 1134 trait correlations found that positive estimates of assortative mating were more frequent and larger in magnitude than negative estimates. Here, we describe the scale-of-choice effect (SCE), which occurs when mate choice exists at a smaller scale than that of the investigator's sampling, while simultaneously the trait is heterogeneously distributed at the true scale-of-choice. We demonstrate the SCE by Monte Carlo simulations and estimate it in two organisms showing positive (Littorina saxatilis) and negative (L. fabalis) assortative mating. Our results show that both positive and negative estimates are biased by the SCE by different magnitudes, typically toward positive values. Therefore, the low frequency of negative assortative mating observed in the literature may be due to the SCE's impact on correlation estimates, which demands new experimental evaluation.
Journal Article
Assortative mating on blood type
Blood type is one of the most fundamental phenotypes in biological, medical, and psychological studies. Using a unique dataset of one million Chinese pregnancies, we find strong evidence from a group of statistical tests for assortative mating on blood type. After controlling for anthropometric and socioeconomic confounders, assortative mating remains robust.
Journal Article
On the Opportunity for Sexual Selection, the Bateman Gradient and the Maximum Intensity of Sexual Selection
Bateman's classic paper on fly mating systems inspired quantitative study of sexual selection but also resulted in much debate and confusion. Here, I consider the meaning of Bateman's principles in the context of selection theory. Success in precopulatory sexual selection can be quantified as a “mating differential,” which is the covariance between trait values and relative mating success. The mating differential is converted into a selection differential by the Bateman gradient, which is the least squares regression of relative reproductive success on relative mating success. Hence, a complete understanding of precopulatory sexual selection requires knowledge of two equally important aspects of mating patterns: the mating differential, which requires a focus on mechanisms generating covariance between trait values and mating success, and the Bateman gradient, which requires knowledge of the genetic mating system. An upper limit on the magnitude of the selection differential on any sexually selected trait is given by the product of the standard deviation in relative mating success and the Bateman gradient. This latter view of the maximum selection differential provides a clearer focus on the important aspects of precopulatory sexual selection than other methods and therefore should be an important part of future studies of sexual selection.
Journal Article
bric à brac controls sex pheromone choice by male European corn borer moths
The sex pheromone system of ~160,000 moth species acts as a powerful form of assortative mating whereby females attract conspecific males with a species-specific blend of volatile compounds. Understanding how female pheromone production and male preference coevolve to produce this diversity requires knowledge of the genes underlying change in both traits. In the European corn borer moth, pheromone blend variation is controlled by two alleles of an autosomal fatty-acyl reductase gene expressed in the female pheromone gland (pgFAR). Here we show that asymmetric male preference is controlled by cis-acting variation in a sex-linked transcription factor expressed in the developing male antenna, bric à brac (bab). A genome-wide association study of preference using pheromone-trapped males implicates variation in the 293 kb bab intron 1, rather than the coding sequence. Linkage disequilibrium between bab intron 1 and pgFAR further validates bab as the preference locus, and demonstrates that the two genes interact to contribute to assortative mating. Thus, lack of physical linkage is not a constraint for coevolutionary divergence of female pheromone production and male behavioral response genes, in contrast to what is often predicted by evolutionary theory.
Journal Article
Stepwise recombination suppression around the mating-type locus associated with a diploid-like life cycle in Schizothecium fungi
Abstract
Recombination suppression often evolves around sex-determining loci and extends stepwise, resulting in adjacent regions with different levels of divergence between sex chromosomes, called evolutionary strata. In Ascomycota fungi, evolutionary strata around the mating-type (MAT) locus have been reported only in pseudo-homothallic species, which have a diploid-like life cycle with mycelia carrying nuclei of both mating types. In contrast, no recombination suppression has been observed in heterothallic fungi, where colonies contain only a single mating type. Here, we investigated the evolution of recombination suppression in a clade of dung fungi encompassing 16 pseudo-homothallic and three heterothallic sibling species from the Schizothecium genus (Ascomycota, Sordariales). The analysis of genetic divergence based on genome sequencing indicated recombination suppression around the MAT locus in all 13 pseudo-homothallic species examined. The nonrecombining region ranged from 600 kb to 1.6 Mb and harbored multiple evolutionary strata, varying in size and number among species. The clustering of alleles according to mating type in gene genealogies, the high linkage disequilibrium, and an inversion in one species supported the lack of recombination in the MAT-proximal region in pseudo-homothallic species. The overall lack of trans-specific polymorphism suggested multiple independent recombination suppression events or occasional recombination/genic conversion. In heterothallic species, progeny analyses showed that recombination occurs in regions at physical distances from the MAT locus similar to those in which it is lacking in the pseudo-homothallic species. We thus revealed here multiple, likely independent evolutionary strata, associated with an extended diploid-like stage in Schizothecium fungi.
Journal Article
A most complex marriage arrangement
Heterostylous genetic polymorphisms provide paradigmatic systems for investigating adaptation and natural selection. Populations are usually comprised of two (distyly) or three (tristyly) mating types, maintained by negative frequency-dependent selection resulting from disassortative mating. Theory predicts that this mating system should result in equal style-morph ratios (isoplethy) at equilibrium. Here, I review recent advances on heterostyly, focusing on examples challenging stereotypical depictions of the polymorphism and unresolved questions. Comparative analyses indicate multiple origins of heterostyly, often within lineages. Ecological studies demonstrate that structural components of heterostyly are adaptations improving the proficiency of animal-mediated cross-pollination and reducing pollen wastage. Both neutral and selective processes cause deviations from isoplethy in heterostylous populations, and, under some ecological and demographic conditions, cause breakdown of the polymorphism, resulting in either the evolution of autogamy and mixed mating, or transitions to alternative outcrossing systems, including dioecy. Earlier ideas on the genetic architecture of the S-locus supergene governing distyly have recently been overturned by discovery that the dominant S-haplotype is a hemizygous region absent from the s-haplotype. Ecological, phylogenetic and molecular genetic data have validated some features of theoretical models on the selection of the polymorphism. Although heterostyly is the best-understood floral polymorphism in angiosperms, many unanswered questions remain.
Journal Article
Trematode Clone Abundance Distributions: An Eco-Evolutionary Link between Parasite Transmission and Parasite Mating Systems
Most trematodes and some cestodes have obligate life history features that include an asexual developmental stage that can produce genetically-identical individuals (clonemates) followed by an adult stage with sexual reproduction. These life history features can influence the evolutionary mechanism of inbreeding in parasites, especially among self-compatible hermaphroditic endoparasites whose mating opportunities are restricted to within hosts. As clonemate mating in hermaphroditic species produces a genetic inbreeding signature identical to that of self-mating, it is important to understand how clonemates are transmitted through their life stages. A handful of prior studies compared clone richness (number of clones) across life cycle stages to infer transmission processes and to characterize clone abundance distributions (CADs) among hosts. Here we illustrate the use of the proportion of clonemate dyads (PC) within hosts to describe the CADs. PC has several advantages as an ecological metric in that it is unbiased by sample size, takes into account relative parasite burdens, and has a direct transmission interpretation, i.e., the probability of cotransmitting clonemates. Moreover, PC is also an evolutionary metric as it can be used to estimate a potential clonemate mating rate. We demonstrate the use of PC in comparing CADs within and across 2 trematode developmental stages in the lancet fluke Dicrocoelium dendriticum. Also, we show how genetic estimates of apparent selfing (true selfing plus clonemate mating) at larval and juvenile stages can be compared to PC estimated at the adult stage to assess the contribution of clonemate mating to apparent selfing. The eco-evolutionary links presented are generalizable to assess sibling cotransmission as well. Thus, the framework presented herein will facilitate future field-based studies on the transmission and mating systems of parasitic flatworms.
Journal Article