The locus of sexual selection: moving sexual selection studies into the post-genomics era.

Sexual selection drives fundamental evolutionary processes such as trait elaboration and speciation. Despite this importance, there are surprisingly few examples of genes unequivocally responsible for variation in sexually selected phenotypes. This lack of information inhibits our ability to predict phenotypic change due to universal behaviours, such as fighting over mates and mate choice. Here, we discuss reasons for this apparent gap and provide recommendations for how it can be overcome by adopting contemporary genomic methods, exploiting underutilized taxa that may be ideal for detecting the effects of sexual selection and adopting appropriate experimental paradigms. Identifying genes that determine variation in sexually selected traits has the potential to improve theoretical models and reveal whether the genetic changes underlying phenotypic novelty utilize common or unique molecular mechanisms. Such a genomic approach to sexual selection will help answer questions in the evolution of sexually selected phenotypes that were first asked by Darwin and can furthermore serve as a model for the application of genomics in all areas of evolutionary biology.

The immunoglobulin heavy chain locus: genetic variation, missing data, and implications for human disease.

The immunoglobulin (IG) loci consist of repeated and highly homologous sets of genes of different types, variable (V), diversity (D) and junction (J), that rearrange in developing B cells to produce an individual's highly variable repertoire of expressed antibodies, designed to bind to a vast array of pathogens. This repeated structure makes these loci susceptible to a high frequency of insertion and deletion events through evolutionary time, and also makes them difficult to characterize at the genomic level or assay with high-throughput techniques. Given the central role of antibodies in the adaptive immune system, it is not surprising that early candidate gene approaches showed that germline polymorphisms in these regions correlated with susceptibility to both infectious and autoimmune diseases. However, more recent studies, particularly those using high-throughput genome-wide arrays, have failed to implicate these loci in disease. In this review of the IG heavy chain variable gene cluster (IGHV), we examine how poorly we understand the distribution of haplotype variation in this genomic region, and we argue that this lack of information may mask candidate loci in the IGHV gene cluster as causative factors for infectious and autoimmune diseases.

Revisiting the T-cell receptor alpha/delta locus and possible associations with multiple sclerosis.

A role for T cells in the pathogenesis of multiple sclerosis (MS) is well supported, evidenced by myriad immunological studies, as well as the unequivocal genetic influence of the major histocompatibility complex (MHC). Despite many attempts, no convincing genetic associations have been made between T-cell receptor (TCR) gene loci and MS. However, these studies may not be definitive because of small sample sizes and under-representative marker coverage of the chromosomal regions being investigated. To explore potential roles between the TCR alpha locus and MS, we have genotyped a large family-based cohort, including 1360 affected individuals and 1659 of their unaffected first-degree relatives, at 40 single-nucleotide polymorphism (SNP) markers within the TCR alpha/delta locus. This represents the largest TCR alpha-MS study to date. From this screen, we identified three potential loci of interest in TCR alpha variable and constant gene regions using the transmission disequilibrium test. Although SNPs implicating each of these regions of interest will require genotyping in independent replication cohorts, these findings suggest a role for TCR gene polymorphisms in MS susceptibility. In the context of these findings we review the evidence.

Sexual isolation and extreme morphological divergence in the Cumana guppy: a possible case of incipient speciation.

Theory predicts that sexual selection can promote the evolution of reproductive isolation and speciation. Those cases in which sexual selection has led to speciation should be characterized by significant differentiation in male display traits and correlated female preferences in the absence of post-zygotic isolation, accompanied by little genetic or other morphological differentiation. Previous evidence indicates that a cluster of populations of the guppy (Poecilia reticulata Peters) from Cumana, Venezuela, the 'Cumana guppy', differs significantly in female preferences from a nearby guppy population (A. Lindholm & F. Breden, Am. Nat., 160: 2002, S214). Here, we further document sexual isolation between these populations. In addition, these populations exhibit significant divergence in male display traits correlated to differences in between-population mating success, little mitochondrial genetic differentiation, and we find no evidence for genetic incompatibility between a Cumana population and several geographically isolated populations. These results suggest that divergent sexual selection has contributed to differentiation of the Cumana guppy, and this may be the first example of incipient speciation in the guppy.

Extreme polymorphism in a Y-linked sexually selected trait.

Males of the livebearing fish, Poecilia parae, exhibit one of the most complex polymorphisms known to occur within populations, whereas females are monomorphic. We describe five distinct male colour morphs and an associated size dimorphism, and demonstrate through pedigree analysis that the locus or loci controlling the male colour polymorphism is linked to the Y-chromosome. Field surveys from 1999 to 2002 of nine populations in Guyana and Suriname, South America, indicate that some morphs are consistently abundant and others are rare, implying that the colour polymorphism has important fitness consequences. By rearing offspring of field-inseminated females, we showed that the common morph is also the most successful morph in terms of reproduction. However, dichotomous choice tests show that two rare morphs are preferred by females over the common morph. These results suggest that alternative male mating strategies, sperm competition, overt male-male competition, or other processes are overriding female preferences in these populations. Furthermore, Y-linkage of the colour polymorphism in P. parae supports the hypothesis that heterogametic sex chromosomes harbour sexually antagonistic traits beneficial to the heterogametic sex.

Slipped-strand mispairing at noncontiguous repeats in Poecilia reticulata: a model for minisatellite birth.

The standard slipped-strand mispairing (SSM) model for the formation of variable number tandem repeats (VNTRs) proposes that a few tandem repeats, produced by chance mutations, provide the "raw material" for VNTR expansion. However, this model is unlikely to explain the formation of VNTRs with long motifs (e.g., minisatellites), because the likelihood of a tandem repeat forming by chance decreases rapidly as the length of the repeat motif increases. Phylogenetic reconstruction of the birth of a mitochondrial (mt) DNA minisatellite in guppies suggests that VNTRs with long motifs can form as a consequence of SSM at noncontiguous repeats. VNTRs formed in this manner have motifs longer than the noncontiguous repeat originally formed by chance and are flanked by one unit of the original, noncontiguous repeat. SSM at noncontiguous repeats can therefore explain the birth of VNTRs with long motifs and the "imperfect" or "short direct" repeats frequently observed adjacent to both mtDNA and nuclear VNTRs.

Slipped-strand mispairing at noncontiguous repeats in Poecilia reticulata: a model for minisatellite birth

The standard slipped-strand mispairing (SSM) model for the formation of variable number tandem repeats (VNTRs) proposes that a few tandem repeats, produced by chance mutations, provide the "raw material" for VNTR expansion. However, this model is unlikely to explain the formation of VNTRs with long motifs (e.g., minisatellites), because the likelihood of a tandem repeat forming by chance decreases rapidly as the length of the repeat motif increases. Phylogenetic reconstruction of the birth of a mitochondrial (mt) DNA minisatellite in guppies suggests that VNTRs with long motifs can form as a consequence of SSM at noncontiguous repeats. VNTRs formed in this manner have motifs longer than the noncontiguous repeat originally formed by chance and are flanked by one unit of the original, noncontiguous repeat. SSM at noncontiguous repeats can therefore explain the birth of VNTRs with long motifs and the "imperfect" or "short direct" repeats frequently observed adjacent to both mtDNA and nuclear VNTRs.

Molecular phylogeny of the live-bearing fish genus Poecilia (Cyprinodontiformes: Poeciliidae).

Members of the genus Poecilia exhibit extensive morphological, behavioral, and life history variation within and between species. This natural variation, coupled with short generation times and the ease with which members of this genus can be cultured in the lab, have made several species model systems for studying the effects of sexual and natural selection on the evolution of natural populations. Given that there is no clear understanding of the phylogenetic relationships within the genus, these studies have not been put into a historical context, and between-species comparisons have been limited. We sequenced the complete NADH Dehydrogenase Subunit 2 (ND2) mitochondrial gene (1047 bp) in representatives of the major divisions of the genus in order to examine these relationships. The subgeneric groups of Rosen and Bailey (1963) are, for the most part, supported, with some adjustment within the subgenera Poecilia and Pamphorichthys. The morphological distinctness of the groups within Poecilia suggest that the original generic designations be reinstated, but this awaits a more thorough analysis. Two implications from the phylogeny are particularly relevant to sexual selection studies: within the North and Central American mollies, the three species of sailfin mollies form a monophyletic group, and within the subgenus Lebistes, the sister taxon to the guppy, P. reticulata, is most likely the group of species previously designated as Micropoecilia.

"Runaway" social evolution: reinforcing selection for inbreeding and altruism.

Kin selection theory predicts that altruistic behaviors, those that decrease the fitness of the individual performing the behavior but increase the fitness of the recipient, can increase in frequency if the individuals interacting are closely related. Several studies have shown that inbreeding therefore generally increases the effectiveness of kin selection when fitnesses are linear, additive functions of the number of altruists in the family, although with extreme forms of altruism, inbreeding can actually retard the evolution of altruism. These models assume that a constant proportion of the population mates at random and a constant proportion practices some form of inbreeding. In order to investigate the effect of inbreeding on the evolution of altruistic behavior when the mating structure is allowed to evolve, we examined a two-locus model by computer simulation of a diploid case and illustrated the important qualitative features by mathematical analysis of a haploid case. One locus determines an individual's propensity to perform altruistic social behavior and the second locus determines the probability that an individual will mate within its sibship. We assumed positive selection for altruism and no direct selection at the inbreeding locus. We observed that the altruistic allele and the inbreeding allele become positively associated, even when the initial conditions of the model assume independence between these loci. This linkage disequilibrium becomes established, because the altruistic allele increases more rapidly in the inbreeding segment of the population. This association subsequently results in indirect selection on the inbreeding locus. However, the dynamics of this model go beyond a simple "hitch-hiking" effect, because high levels of altruism lead to increased inbreeding, and high degrees of inbreeding accelerate the rate of change of the altruistic allele in the entire population. Thus, the dynamics of this model are similar to those of "runaway" sexual selection, with gene frequency change at the two loci interactively causing rapid evolutionary change.

Partitioning of covariance as a method for studying kin selection.

Covariance models of selection predict gene frequency change in terms of the relationship between the fitness of an individual and its phenotype, and therefore provide a convenient method for studying evolution in natural systems. When these models are partitioned into effects acting within and between hierarchical levels of selection, they can be directly applied to questions of kin selection. In many cases, the partitioning of covariance approach to the study of kin selection is a more useful alternative to the traditional hamiltonian or inclusive fitness approach.