Female alternative reproductive tactics: diversity and drivers.

It is often argued that anisogamy causes alternative reproductive tactics (ARTs) to be more common in males than females. We challenge this view by pointing out logical flaws in the argument. We then review recent work on the diversity of female ARTs, listing several understudied types such as solitary versus communal breeding and facultative parthenogenesis. We highlight an important difference between male and female ARTs that caused female ARTs to be overlooked: male ARTs tend to focus on successful fertilization, whereas female ARTs occur at many stages of reproduction and often form complex networks of decision points. We propose to study correlated female ARTs as a whole to better understand their drivers and eco-evolutionary dynamics.

Has recombination changed during the recent evolution of the guppy Y chromosome?

Genome sequencing and genetic mapping of molecular markers have demonstrated nearly complete Y-linkage across much of the guppy (Poecilia reticulata) XY chromosome pair. Predominant Y-linkage of factors controlling visible male-specific coloration traits also suggested that these polymorphisms are sexually antagonistic (SA). However, occasional exchanges with the X are detected, and recombination patterns also appear to differ between natural guppy populations, suggesting ongoing evolution of recombination suppression under selection created by partially sex-linked SA polymorphisms. We used molecular markers to directly estimate genetic maps in sires from 4 guppy populations. The maps are very similar, suggesting that their crossover patterns have not recently changed. Our maps are consistent with population genomic results showing that variants within the terminal 5 Mb of the 26.5 Mb sex chromosome, chromosome 12, are most clearly associated with the maleness factor, albeit incompletely. We also confirmed occasional crossovers proximal to the male-determining region, defining a second, rarely recombining, pseudo-autosomal region, PAR2. This fish species may therefore have no completely male-specific region (MSY) more extensive than the male-determining factor. The positions of the few crossover events suggest a location for the male-determining factor within a physically small repetitive region. A sex-reversed XX male had few crossovers in PAR2, suggesting that this region's low crossover rate depends on the phenotypic, not the genetic, sex. Thus, rare individuals whose phenotypic and genetic sexes differ, and/or occasional PAR2 crossovers in males can explain the failure to detect fully Y-linked variants.

Partial sex linkage and linkage disequilibrium on the guppy sex chromosome.

The guppy Y chromosome has been considered a model system for the evolution of suppressed recombination between sex chromosomes, and it has been proposed that complete sex-linkage has evolved across about 3 Mb surrounding this fish's sex-determining locus, followed by recombination suppression across a further 7 Mb of the 23 Mb XY pair, forming younger "evolutionary strata". Sequences of the guppy genome show that Y is very similar to the X chromosome. Knowing which parts of the Y are completely nonrecombining, and whether there is indeed a large completely nonrecombining region, are important for understanding its evolution. Here, we describe analyses of PoolSeq data in samples from within multiple natural populations from Trinidad, yielding new results that support previous evidence for occasional recombination between the guppy Y and X. We detected recent demographic changes, notably that downstream populations have higher synonymous site diversity than upstream ones and other expected signals of bottlenecks. We detected evidence of associations between sequence variants and the sex-determining locus, rather than divergence under a complete lack of recombination. Although recombination is infrequent, it is frequent enough that associations with SNPs can suggest the region in which the sex-determining locus must be located. Diversity is elevated across a physically large region of the sex chromosome, conforming to predictions for a genome region with infrequent recombination that carries one or more sexually antagonistic polymorphisms. However, no consistently male-specific variants were found, supporting the suggestion that any completely sex-linked region may be very small.

Sensory-based quantification of male colour patterns in Trinidadian guppies reveals no support for parallel phenotypic evolution in multivariate trait space.

Parallel evolution, in which independent populations evolve along similar phenotypic trajectories, offers insights into the repeatability of adaptive evolution. Here, we revisit a classic example of parallelism, that of repeated evolution of brighter males in the Trinidadian guppy (Poecilia reticulata). In guppies, colonisation of low predation habitats is associated with emergence of 'more colourful' phenotypes since predator-induced viability selection for crypsis weakens while sexual selection by female preference for conspicuousness remains strong. Our study differs from previous investigations in three respects. First, we adopted a multivariate phenotyping approach to characterise parallelism in multitrait space. Second, we used ecologically-relevant colour traits defined by the visual systems of the two selective agents (i.e., guppy, predatory cichlid). Third, we estimated population genetic structure to test for adaptive (parallel) evolution against a model of neutral phenotypic divergence. We find strong phenotypic differentiation that is inconsistent with a neutral model but very limited support for the predicted pattern of greater conspicuousness at low predation. Effects of predation regime on each trait were in the expected direction, but weak, largely nonsignificant, and explained little among-population variation. In multitrait space, phenotypic trajectories of lineages colonising low from high predation regimes were not parallel. Our results are consistent with reduced predation risk facilitating adaptive differentiation, potentially by female choice, but suggest that this proceeds in independent directions of multitrait space across lineages. Pool-sequencing data also revealed SNPs showing greater differentiation than expected under neutrality, among which some are found in genes contributing to colour pattern variation, presenting opportunities for future genetic study.

Nuclear androgen and progestin receptors inversely affect aggression and social dominance in male zebrafish (Danio rerio).

Aggression is a fundamental behavior displayed universally among animal species, but hyper- or hypo-aggressiveness can be maladaptive with negative consequences for individuals and group members. While the social and ecological significance of aggression is well understood, the specific neurobiological and hormonal mechanisms responsible for mediating aggression have not been fully elucidated. Previous studies have shown a relationship between aggressive acts and circulating gonadal steroids, but whether classical nuclear steroid receptors regulate aggression in animals is still uncertain. We examined whether the nuclear androgen receptor (Ar) and nuclear progestin receptor (Pgr) were necessary for aggressive behaviors and maintenance of a dominance relationship in male zebrafish (Danio rerio). Dyadic social interactions of Ar knockout (ArKO), Pgr knockout (PgrKO) and wildtype (WT) controls were observed for two weeks (2-weeks). ArKO zebrafish were significantly less aggressive and had a less defined dominance relationship, whereas PgrKO dominant zebrafish were significantly and persistently more aggressive with a robust dominance relationship. Our results demonstrate the importance of nuclear steroid hormone receptors in regulating aggression of adult male zebrafish and provide new models for understanding of the mechanisms of aggression.

Locating the Sex Determining Region of Linkage Group 12 of Guppy (Poecilia reticulata).

Despite over 100 years of study, the location of the fully sex-linked region of the guppy (Poecilia reticulata) carrying the male-determining locus, and the regions where the XY pair recombine, remain unclear. Previous population genomics studies to determine these regions used small samples from recently bottlenecked captive populations, which increase the false positive rate of associations between individuals' sexes and SNPs. Using new data from multiple natural populations, we show that a recently proposed candidate for this species' male-determining gene is probably not completely sex-linked, leaving the maleness factor still unidentified. Variants in the chromosome 12 region carrying the candidate gene sometimes show linkage disequilibrium with the sex-determining factor, but no consistently male-specific variant has yet been found. Our genetic mapping with molecular markers spread across chromosome 12 confirms that this is the guppy XY pair. We describe two families with recombinants between the X and Y chromosomes, which confirm that the male-determining locus is in the region identified by all previous studies, near the terminal pseudo-autosomal region (PAR), which crosses over at a very high rate in males. We correct the PAR marker order, and assign two unplaced scaffolds to the PAR. We also detect a duplication, with one copy in the male-determining region, explaining signals of sex linkage in a more proximal region.

Using GC Content to Compare Recombination Patterns on the Sex Chromosomes and Autosomes of the Guppy, Poecilia reticulata, and Its Close Outgroup Species.

Genetic and physical mapping of the guppy (Poecilia reticulata) have shown that recombination patterns differ greatly between males and females. Crossover events occur evenly across the chromosomes in females, but in male meiosis they are restricted to the tip furthest from the centromere of each chromosome, creating very high recombination rates per megabase, as in pseudoautosomal regions of mammalian sex chromosomes. We used GC content to indirectly infer recombination patterns on guppy chromosomes, based on evidence that recombination is associated with GC-biased gene conversion, so that genome regions with high recombination rates should be detectable by high GC content. We used intron sequences and third positions of codons to make comparisons between sequences that are matched, as far as possible, and are all probably under weak selection. Almost all guppy chromosomes, including the sex chromosome (LG12), have very high GC values near their assembly ends, suggesting high recombination rates due to strong crossover localization in male meiosis. Our test does not suggest that the guppy XY pair has stronger crossover localization than the autosomes, or than the homologous chromosome in the close relative, the platyfish (Xiphophorus maculatus). We therefore conclude that the guppy XY pair has not recently undergone an evolutionary change to a different recombination pattern, or reduced its crossover rate, but that the guppy evolved Y-linkage due to acquiring a male-determining factor that also conferred the male crossover pattern. We also identify the centromere ends of guppy chromosomes, which were not determined in the genome assembly.

Convergent evolution of body color between sympatric freshwater fishes via different visual sensory evolution.

Although there are many examples of color evolution potentially driven by sensory drive, only few studies have examined whether distinct species inhabiting the same environments evolve similar body colors via shared sensory mechanisms. In this study, we tested whether two sympatric freshwater fish taxa, halfbeaks of the genus Nomorhamphus and ricefishes of the genus Oryzias in Sulawesi Island, converge in both body color and visual sensitivity. After reconstructing the phylogeny separately for Nomorhamphus and Oryzias using transcriptome-wide sequences, we demonstrated positive correlations of body redness between these two taxa across environments, even after phylogenetic corrections, which support convergent evolution. However, substantial differences were observed in the expression profiles of opsin genes in the eyes between Nomorhamphus and Oryzias. Particularly, the expression levels of the long wavelength-sensitive genes were negatively correlated between the taxa, indicating that they have different visual sensitivities despite living in similar light environments. Thus, the convergence of body colorations between these two freshwater fish taxa was not accompanied by convergence in opsin sensitivities. This system presents a case in which body color convergence can occur between sympatric species via different mechanisms.

Exaggerated heterochiasmy in a fish with sex-linked male coloration polymorphisms.

It is often stated that polymorphisms for mutations affecting fitness of males and females in opposite directions [sexually antagonistic (SA) polymorphisms] are the main selective force for the evolution of recombination suppression between sex chromosomes. However, empirical evidence to discriminate between different hypotheses is difficult to obtain. We report genetic mapping results in laboratory-raised families of the guppy (Poecilia reticulata), a sexually dimorphic fish with SA polymorphisms for male coloration genes, mostly on the sex chromosomes. Comparison of the genetic and physical maps shows that crossovers are distributed very differently in the two sexes (heterochiasmy); in male meiosis, they are restricted to the termini of all four chromosomes studied, including chromosome 12, which carries the sex-determining locus. Genome resequencing of male and female guppies from a population also indicates sex linkage of variants across almost the entire chromosome 12. More than 90% of the chromosome carrying the male-determining locus is therefore transmitted largely through the male lineage. A lack of heterochiasmy in a related fish species suggests that it originated recently in the lineage leading to the guppy. Our findings do not support the hypothesis that suppressed recombination evolved in response to the presence of SA polymorphisms. Instead, a low frequency of recombination on a chromosome that carries a male-determining locus and has not undergone genetic degeneration has probably facilitated the establishment of male-beneficial coloration polymorphisms.

Variation in female aggression in 2 three-spined stickleback populations with female throat and spine coloration.

Despite growing interest in female ornament evolution, we still have a rudimentary understanding of female display traits relative to similar traits in males. Under one popular adaptive scenario, female ornaments are hypothesized to function in female-female competition and serve as badges of status, such that their expression is linked with elevated aggression in some cases. In this study, we investigated the relationship between 2 female ornaments-male-like red throat color and red spine coloration-and female aggression in 2 independently derived stream-resident populations of three-spined stickleback Gasterosteus aculeatus. Using simulated intrusions, we tested whether females with redder ornaments were generally more aggressive, and for variation in aggressive and social behaviors between the 2 populations. We found that the red intensity of the throat and spine did not predict aggression levels in either population, suggesting a limited role for both female ornaments during female-female interaction. The 2 populations exhibited different levels of aggressive behaviors, unrelated to the color patches. Our results suggest that variation in selective pressures between populations may promote interpopulation variance in aggressive behavior but not the correlation between female ornamentation and aggression, and raise the possibility that red coloration may have evolved through different mechanisms or processes in the 2 populations.

Local adaptation and the evolution of inversions on sex chromosomes and autosomes.

Spatially varying selection with gene flow can favour the evolution of inversions that bind locally adapted alleles together, facilitate local adaptation and ultimately drive genomic divergence between species. Several studies have shown that the rates of spread and establishment of new inversions capturing locally adaptive alleles depend on a suite of evolutionary factors, including the strength of selection for local adaptation, rates of gene flow and recombination, and the deleterious mutation load carried by inversions. Because the balance of these factors is expected to differ between X (or Z) chromosomes and autosomes, opportunities for inversion evolution are likely to systematically differ between these genomic regions, though such scenarios have not been formally modelled. Here, we consider the evolutionary dynamics of X-linked and autosomal inversions in populations evolving at a balance between migration and local selection. We identify three factors that lead to asymmetric rates of X-linked and autosome inversion establishment: (1) sex-biased migration, (2) dominance of locally adapted alleles and (3) chromosome-specific deleterious mutation loads. This theory predicts an elevated rate of fixation, and depressed opportunities for polymorphism, for X-linked inversions. Our survey of data on the genomic distribution of polymorphic and fixed inversions supports both theoretical predictions.This article is part of the theme issue 'Linking local adaptation with the evolution of sex differences'.

Phylogenomics reveals habitat-associated body shape divergence in Oryzias woworae species group (Teleostei: Adrianichthyidae).

The Oryzias woworae species group, composed of O. asinua, O. wolasi, and O. woworae, is widely distributed in southeastern Sulawesi, an island in the Indo-Australian Archipelago. Deep-elongated body shape divergence is evident among these three species to the extent that it is used as a species-diagnostic character. These fishes inhabit a variety of habitats, ranging from upper streams to ponds, suggesting that the body shape divergence among the three species may reflect adaptation to local environments. First, our geometric morphometrics among eight local populations of this species group revealed that the three species cannot be separated by body shape and that riverine populations had more elongated bodies and longer caudal parts than lacustrine populations. Second, their phylogenetic relationships did not support the presence of three species; phylogenies using mitochondrial DNA and genomic data obtained from RNA-Seq revealed that the eight populations could not be sorted into three different clades representing three described species. Third, phylogenetic corrections of body shape variations and ancestral state reconstruction of body shapes demonstrated that body shape divergence between riverine and lacustrine populations persisted even if the phylogenies were considered and that body shape evolved rapidly irrespective of phylogeny. Sexual dimorphism in body shape was also evident, but the degree of dimorphism did not significantly differ between riverine and lacustrine populations after phylogenetic corrections, suggesting that sexual selection may not substantially contribute to geographical variations in body shape. Overall, these results indicate that the deep-elongated body shape divergence of the O. woworae species group evolved locally in response to habitat environments, such as water currents, and that a thorough taxonomic reexamination of the O. woworae species group may be necessary.

Genetic editing of the androgen receptor contributes to impaired male courtship behavior in zebrafish.

Elucidating the genes that contribute to behavioral variation has become an important endeavor in behavioral studies. While advances in genomics have narrowed down the list of candidate genes, functional validation of them has lagged behind, partly because of challenges associated with rapid gene manipulations. Consequently, few studies have demonstrated causal genetic changes linked to behaviors. The 'gene editing revolution' has offered unprecedented opportunities to investigate candidate genes responsible for critical behaviors. Here, we edited the androgen receptor gene (AR), which is associated with male reproductive behavior in zebrafish, using TAL effector nucleases (TALENs), and tested whether modifications at the AR impacted courtship during mating trials. We reveal that males lacking AR courted females significantly less, showing reduced levels of stereotypic behaviors. Consistent with previous studies, disrupting androgen mechanisms can lead to behavioral changes with potential fitness consequences. Our study highlights the possibility of genetically altering a reproductive behavior, further solidifying the link between genotype and behavior.

Genetic Architecture of Conspicuous Red Ornaments in Female Threespine Stickleback.

Explaining the presence of conspicuous female ornaments that take the form of male-typical traits has been a longstanding challenge in evolutionary biology. Such female ornaments have been proposed to evolve via both adaptive and nonadaptive evolutionary processes. Determining the genetic underpinnings of female ornaments is important for elucidating the mechanisms by which such female traits arise and persist in natural populations, but detailed information about their genetic basis is still scarce. In this study, we investigated the genetic architecture of two ornaments, the orange-red throat and pelvic spine, in the threespine stickleback (Gasterosteus aculeatus). Throat coloration is male-specific in ancestral marine populations but has evolved in females in some derived stream populations, whereas sexual dimorphism in pelvic spine coloration is variable among populations. We find that ornaments share a common genetic architecture between the sexes. At least three independent genomic regions contribute to red throat coloration, and harbor candidate genes related to pigment production and pigment cell differentiation. One of these regions is also associated with spine coloration, indicating that both ornaments might be mediated partly via pleiotropic genetic mechanisms.