Phylogenetic analyses of primate size evolution: the consequences of sexual selection

We have analysed the relationship between primate mating system, size and size dimorphism by utilizing several phylogenetically based methods. An independent contrast analysis of male and female size (log weight) showed that these are tightly correlated and that size dimorphism is not a simple allometric function of size. We found no relationship between mating system and sexual dimorphism in strepsirhines but a strong relationship in haplorhines. By matched-pairs analysis, where sister groups were matched according to whether the mating system predicted higher or lower intrasexual selection for male size, haplorhine species in more polygynous clades (with a predicted higher sexual selection) were significantly more dimorphic, had larger males, and also, but to a lesser degree, larger females. Both independent contrast and matched-pairs analyses are non-directional and correlational. By using a directional test we investigated how a transition in mating system affects size and dimorphism. Here, each observation is the sum of changes in dimorphism or size in a clade that is defined by a common origin of a mating system. Generally, dimorphism, as well as male and female size, increased after an expected increase in sexual selection, and decreased after an expected decrease in sexual selection. The pattern was, however, not significant for all of the alternative character reconstructions. In clades with an expected increase in sexual selection, male size increased more than female size. This pattern was significant for all character reconstructions. The directional investigation indicates that the magnitude of change in haplorhine dimorphism is larger after an increase in sexual selection than after a decrease, and, for some reconstructions, that the magnitude of size increase is larger than the magnitude of size decrease for both sexes. Possible reasons for these patterns are discussed, as well as their implications as being one possible mechanism behind Cope's rule, i.e. general size increase in many phylogenetic lineages.     

Phylogenetic models and model selection for noncoding DNA

Awareness of the complex structure and evolutionary dynamics of noncoding DNA has improved both noncoding sequence alignment and the use of microstructural changes as characters in phylogenetic analysis. The next step is to consider improvements in the use and selection of phylogenetic models for noncoding sequence data. Models of character evolution are central to phylogeny estimation, but the use of an inadequate model can mislead topology selection and branch length estimations. This is particularly likely when sequence divergence is either limited (nearly invariable, as in population-level or species-level studies) or extreme (nearly saturated, as in deep-level studies that focus on conserved secondary structures). Noncoding data sets are often at these extremes, and they can be particularly awkward for model definition and model selection. This paper introduces the goals of model use in phylogenetics and identifies ten issues that arise from the application of models to noncoding sequence data. It is concluded that most of these issues derive from small data set sizes, very low or very high sequence variability, limitations of current phylogenetic models, and possibly character definition and nonindependence. Recommendations are made that should help to improve alignment, character quality, model selection, and phylogeny estimation based on noncoding sequence data.     

Fisher's lost model of runaway sexual selection

The bizarre elaboration of sexually selected traits such as the peacock's tail was a puzzle to Charles Darwin and his 19th century followers. Ronald A. Fisher crafted an ingenious solution in the 1930s, positing that female preferences would become genetically correlated with preferred traits due to nonrandom mating. These genetic correlations would translate selection for preferred traits into selection for stronger preferences, leading to a self-reinforcing process of ever-elaborating traits and preferences. It is widely believed that Fisher provided only a verbal model of this “runaway” process. However, in correspondence with Charles Galton Darwin, Fisher also laid out a simple mathematical model that purportedly confirms his verbal prediction of runaway sexual selection. Unfortunately, Fisher's model contains inconsistencies that render his quantitative conclusions inaccurate. Here, we correct Fisher's model and show that it contains all the ingredients of a working runaway process. We derive quantitative predictions of his model using numerical techniques that were unavailable in Fisher's time. Depending on parameter values, mean traits and preferences may increase until genetic variance is depleted by selection, exaggerate exponentially while their variances remain stable, or both means and variances may increase super-exponentially. We thus present the earliest mathematical model of runaway sexual selection.     

A sexual selection model for hominid evolution

The following paper develops a sexual selection model for the evolution of bipedal locomotion, canine reduction, brain enlargement, language and higher intelligence. The model involves an expansion of Darwin’s ideas about human evolution based on recent elaborations of sexual selection theory. Modern notions about intrasexual competition and female and male choice and their ecological correlates are summarized along with a new model for the role of sexual selection in speciation. Rapid evolution of bipedal locomotion as a male adaptation for nuptial feeding of females is proposed as a model for ape-hominid divergence through sexual selection; canine reduction is attributed to selection for associated epigamic displays. The analogy with male specialization through sexual selection speciation in hamadryas baboons is noted. Subsequent changes in female reproductive physiology are attributed to female competition for increased male parental investment during the time of early Homo andHomo erectus. The origin of higher intellectual and language abilities inHomo sapiens is attributed to male competition through technology and rule production to control resources and females; intellectual abilities involved in social manipulation are attributed to female competition for male parental investment and maintenance of polyandry. The course of hominid evolution is characterized as involving a trend from a promiscuous mating system toward increasing intensity of adaptations for male control of females, and by increasing intensity of female adaptation to maintain male parental investment while circumventing male control.     

Frequency dependence in a model of sexual selection

A model of sexual selection is studied, in which females mate with males chosen out of a group of males. Group size may vary for different females. Males are of two kinds, more and less attractive, with the more attractive form having a higher chance of succeeding in mating with the females. It is shown by considering the realised fecundities of the two types of males, at different frequencies in the population, that protected polymorphism for a locus controlling the male type is possible. However, it requires strong sexual selection and a distribution of group sizes with a high variance. In many cases, although there is frequency dependence, it acts to increase the advantage of the preferred form, as it increases in frequency.     

Sensory exploitation and sexual conflict

Much of the literature on male-female coevolution concerns the processes by which male traits and female preferences for these can coevolve and be maintained by selection. There has been less explicit focus on the origin of male traits and female preferences. Here, I argue that it is important to distinguish origin from subsequent coevolution and that insights into the origin can help us appreciate the relative roles of various coevolutionary processes for the evolution of diversity in sexual dimorphism. I delineate four distinct scenarios for the origin of male traits and female preferences that build on past contributions, two of which are based on pre-existing variation in quality indicators among males and two on exploitation of pre-existing sensory biases among females. Recent empirical research, and theoretical models, suggest that origin by sensory exploitation has been widespread. I argue that this points to a key, but perhaps transient, role for sexually antagonistic coevolution (SAC) in the subsequent evolutionary elaboration of sexual traits, because (i) sensory exploitation is often likely to be initially costly for individuals of the exploited sex and (ii) the subsequent evolution of resistance to sensory exploitation should often be associated with costs due to selective constraints. A review of a few case studies is used to illustrate these points. Empirical data directly relevant to the costs of being sensory exploited and the costs of evolving resistance is largely lacking, and I stress that such data would help determining the general importance of sexual conflict and SAC for the evolution of sexual dimorphism.     

Intralocus sexual conflict diminishes the benefits of sexual selection

Evolution based on the benefits of acquiring “good genes” in sexual selection is only plausible with the reliable transmission of genetic quality from one generation to the next. Accumulating evidence suggests that sexually antagonistic (SA) genes with opposite effects on Darwinian fitness when expressed in the two different sexes may be common in animals and plants. These SA genes should weaken the potential indirect genetic benefits of sexual selection by reducing the fitness of opposite-sex progeny from high-fitness parents. Here we use hemiclonal analysis in the fruit fly, Drosophila melanogaster, to directly measure the inheritance of fitness across generations, over the entire genome. We show that any potential genetic benefits of sexual selection in this system are not merely weakened, but completely reversed over one generation because high-fitness males produce low-fitness daughters and high-fitness mothers produce low-fitness sons. Moreover, male fitness was not inherited by sons, consistent with both theory and recent evidence connecting this form of SA variation with the X chromosome. This inheritance pattern may help to explain how genetic variation for fitness is sustained despite strong sexual selection, and why the ZW sex chromosome system found in birds and butterflies appears to foster the evolution of extreme secondary sexual characters in males.     

Frequency-dependent sexual selection

Sexual selection by female choice is expected to give rise to a frequency-dependent sexual advantage in favour of preferred male phenotypes: the rarer the preferred phenotypes, the more often they are chosen as mates. This 'rare-male advantage' can maintain a polymorphism when two or more phenotypes are mated preferentially: each phenotype gains an advantage when it is rarer than the others; no preferred phenotype can then be lost from the population. Expression of preference may be complete or partial. In models of complete preference, females with a preference always mate preferentially. Models of partial preference are more realistic: in these models, the probability that a female mates preferentially depends on the frequency with which she encounters the males she prefers. Two different 'encounter models' of partial preference have been derived: the O'Donald model and the Charlesworth model. The encounter models contain the complete preference model as a limiting case. In this paper, the Charlesworth model is generalized to allow for female preference of more than one male phenotype. Levels of frequency dependence can then be compared in the O'Donald and Charlesworth models. The complete preference model and both encounter models are formulated in the same genetical terms of preferences for dominant and recessive male phenotypes. Polymorphic equilibria and conditions for stability are derived for each of the three models. The models are then fitted to data of frequencies of matings observed in experiments with the two-spot ladybird. The complete preference model gives as good a fit as the encounter models to the data of these and other experiments. The O'Donald and Charlesworth encounter models are shown to produce a very similar frequency-dependent relation. Generally, as females become less choosy, they express their preference with more dependence on male frequency, whereas the resulting selection of the males becomes less frequency dependent. More choosy females are more constant in expressing their preference, producing greater frequency dependence in the selection of the males.     

Postcopulatory sexual selection

The female reproductive tract is where competition between the sperm of different males takes place, aided and abetted by the female herself. Intense postcopulatory sexual selection fosters inter-sexual conflict and drives rapid evolutionary change to generate a startling diversity of morphological, behavioural and physiological adaptations. We identify three main issues that should be resolved to advance our understanding of postcopulatory sexual selection. We need to determine the genetic basis of different male fertility traits and female traits that mediate sperm selection; identify the genes or genomic regions that control these traits; and establish the coevolutionary trajectory of sexes.     

A deterministic genetic model for sympatric speciation by sexual selection

A deterministic haploid genetic model confirms and explores in more detail the results of our previous individual-based simulation model for sympatric speciation by sexual selection. With the deterministic model, we are able to elucidate parameter dependence by phase plane analysis. We clarify how and why sympatric speciation by sexual selection can happen in a number of ways: (1) Female preferences for or against particular types of males have different effects. Whereas the former affects how readily speciation is invoked, the latter changes the stability of speciation equilibrium. (2) When there is no cost on male ornamentations, speciation is triggered regardless of initial haplotype frequencies if sufficient female preference is provided. (3) There exists a threshold for female initial frequencies for speciation to be invoked, but male initial frequencies have little effect. (4) A small cost on female mate choice does not cancel speciation, but when large, it greatly reduces the possibility of speciation.     

Domesticated birds as a model for the genetics of speciation by sexual selection

In theory, even populations occupying identical environments can diverge in sexually selected traits, as a consequence of different mutational input. I evaluate the potential of this process by comparing the genetics of breeds of domesticated birds to what is known about the genetics of differences among species. Within domesticated species there is a strong correlation of time since domestication with the number of breeds. Descendants of the rock dove, Columba livia (the oldest domesticate) show differences in courtship, vocalizations, body shape, feather ornaments (crests and tails) and colors and color patterns. When nine other domesticated species are included there is a striking hierarchy, with more recent domesticates having a nested subset of these traits: the youngest domesticated species have breeds distinguished only by color. This suggests that selection of new, visible, mutations is driving the process of breed diversification, with mutations that appeal to the breeder happening the most frequently in color. In crosses among related species, color, feather ornaments and many vocalizations and displays show both intermediate dominance and pure dominance. Although the number of loci affecting each of these traits is typically unknown, limited evidence of the genetics of species differences suggests that some differences are due to the substitution of single genes of major effect. While neither the genetics of breeds nor the genetics of species provide a perfect model for the genetics of speciation, similarities between the two are sufficiently striking to infer that major, visible, mutations can provide the impetus underlying new directions of sexual selection.     

On Richerson and Boyd's model of cultural evolution by sexual selection

Richerson and Boyd proposed a model of sexual selection in which both the male trait and the female preference are culturally transmitted. We generalize their model by introducing sex-dependent oblique transmission rates and a fairly comprehensive female preference rule. The model differs markedly from the standard genetic models in that the male trait and the female preference are uncorrelated. Hence, there can be no "sexy son" effect to offset the assumed fertility cost to choosy females. Nevertheless, the cultural processes can support a stable polymorphic equilibrium at which the choosy females are present. Also of interest are the cyclical dynamics observed in the neighborhood of the internal equilibrium.     

Predicting the direction of sexual selection

Our current understanding of the operation of sexual selection is predicated on a sex difference in parental investment, which favours one sex becoming limiting and choosy over mates, the other competitive and nonchoosy. This difference is reflected in the operational sex ratio (OSR), the ratio of sexually receptive males to females, considered to be of fundamental importance in predicting the direction of sexual selection. Difficulties in measuring OSR directly have led to the use of the potential reproductive rates (PRR) as a measure of the level of investment in offspring of males and females. Several recent studies have emphasized that other factors, such as variation in mate quality and sex differences in mortality patterns, also influence the direction of sexual selection. However, as yet there has been no attempt to form a comprehensive theory of sex roles. Here we show that neither OSR nor PRR is the most fundamentally important determinant of sex roles, and that they are not interchangeable. Instead, the cost of a single breeding attempt has a strong direct effect on competition and choosiness as well as consistent relationships to both OSR and PRR. Our life history based approach to mate choice also yields simple, testable predictions on lack of choice in either sex and on mutual mate choice.     

Theories of sexual selection

Recent research on sexual selection in animals has begun to indicate that 'handicaps' and 'honest signalling' may play more important roles than hitherto thought. This review reappraises theories of sexual selection in the light of these new developments.