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.

Can a Y Chromosome Degenerate in an Evolutionary Instant? A Commentary on Fong et al. 2023.

It is well known that the Y chromosomes of Drosophila and mammals and the W chromosomes of birds carry only small fractions of the genes carried by the homologous X or Z chromosomes, and this "genetic degeneration" is associated with loss of recombination between the sex chromosome pair. However, it is still not known how much evolutionary time is needed to reach such nearly complete degeneration. The XY pair of species in a group of closely related poecilid fish is homologous but has been found to have either nondegenerated or completely degenerated Y chromosomes. We evaluate evidence described in a recent paper and show that the available data cast doubt on the view that degeneration has been extraordinarily rapid in the latter (Micropoecilia species).

Novel host unmasks heritable variation in plant preference within an insect population.

Introductions of novel plant species can disturb the historical resource environment of herbivorous insects, resulting in strong selection to either adopt or exclude the novel host. However, an adaptive response depends on heritable genetic variation for preference or performance within the targeted herbivore population, and it is unclear how heritability of host-use preference may differ between novel and historical hosts. Pieris macdunnoughii butterflies in the Rocky Mountains lay eggs on the nonnative mustard Thlaspi arvense, which is lethal to their offspring. Heritability analyses revealed considerable sex-linked additive genetic variation in host preference within a population of this butterfly. This was contrary to general predictions about the genetic basis of preference variation, which are hypothesized to be sex linked between populations but autosomal within populations. Evidence of sex linkage disappeared when butterflies were tested on methanol-based chemical extracts, suggesting these chemicals in isolation may not be the primary driver of female choice among available host plants. Although unexpected, evidence for within-population sex-linked genetic variation in preference for T. arvense over native hosts indicates that persistent maladaptive oviposition on this lethal plant must be maintained by alternative evolutionary dynamics such as migration- or drift-selection balance or pleiotropic constraints.

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.

Autosomal, sex-linked and mitochondrial loci resolve evolutionary relationships among wrens in the genus Campylorhynchus.

Although there is general consensus that sampling of multiple genetic loci is critical in accurate reconstruction of species trees, the exact numbers and the best types of molecular markers remain an open question. In particular, the phylogenetic utility of sex-linked loci is underexplored. Here, we sample all species and 70% of the named diversity of the New World wren genus Campylorhynchus using sequences from 23 loci, to evaluate the effects of linkage on efficiency in recovering a well-supported tree for the group. At a tree-wide level, we found that most loci supported fewer than half the possible clades and that sex-linked loci produced similar resolution to slower-coalescing autosomal markers, controlling for locus length. By contrast, we did find evidence that linkage affected the efficiency of recovery of individual relationships; as few as two sex-linked loci were necessary to resolve a selection of clades with long to medium subtending branches, whereas 4-6 autosomal loci were necessary to achieve comparable results. These results support an expanded role for sampling of the avian Z chromosome in phylogenetic studies, including target enrichment approaches. Our concatenated and species tree analyses represent significant improvements in our understanding of diversification in Campylorhynchus, and suggest a relatively complex scenario for its radiation across the Miocene/Pliocene boundary, with multiple invasions of South America.

With or Without W? Molecular and Cytogenetic Markers are Not Sufficient for Identification of Environmentally-Induced Sex Reversal in the Bearded Dragon.

Transitions from environmental sex determination (ESD) to genotypic sex determination (GSD) require an intermediate step of sex reversal, i.e., the production of individuals with a mismatch between the ancestral genotypic and the phenotypic sex. Among amniotes, the sole well-documented transition in this direction was shown in the laboratory in the central bearded dragon, Pogona vitticeps, where very high incubation temperatures led to the production of females with the male-typical (ZZ) genotype. These sex-reversed females then produced offspring whose sex depended on the incubation temperature. Sex-reversed animals identified by molecular and cytogenetic markers were also reported in the field, and their increasing incidence was speculated as a climate warming-driven transition in sex determination. We show that the molecular and cytogenetic markers normally sex-linked in P. vitticeps are also sex-linked in P. henrylawsoni and P. minor, which points to quite ancient sex chromosomes in this lineage. Nevertheless, we demonstrate, based on a crossing experiment with a male bearded dragon who possesses a mismatch between phenotypic sex and genotype, that the used cytogenetic and molecular markers might not be reliable for the identification of sex reversal. Sex reversal should not be considered as the only mechanism causing a mismatch between genetic sex-linked markers and phenotypic sex, which can emerge also by other processes, here most likely by a rare recombination between regions of sex chromosomes which are normally sex-linked. We warn that sex-linked, even apparently for a long evolutionary time, and sex-specific molecular and cytogenetic markers are not a reliable tool for the identification of sex-reversed individuals in a population and that sex reversal has to be verified by other approaches, particularly by observation of the sex ratio of the progeny.

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.

Cross-species utility of microsatellite loci for the genetic characterisation of Anisakis berlandi (Nematoda: Anisakidae).

Eight microsatellite loci, recently developed in the species Anisakis pegreffii, were successfully amplified in Anisakis berlandi, sibling species of the A. simplex (s. l.) complex. They were validated on adult specimens (n = 46) of the parasite species, collected from two individuals of the definitive host, the long-finned pilot whale Globicephala melas from New Zealand waters. Among the eight loci scored, one, Anisl 07132, had null alleles in A. berlandi and was thus excluded from the subsequent genetic analysis. Two loci, Anisl 00314 and Anisl 10535, were monomorphic. In addition, as also previously detected in the other species of the A. simplex (s. l.) complex, the Anisl 7 locus was seen to be sex-linked, showing hemizygosity in male specimens. Differential allele frequency distributions of A. berlandi, with respect to those previously observed in A. pegreffii and A. simplex (s. s.), were found at some microsatellite loci. The Anisl 7 locus provided 100% diagnosis between A. berlandi and A. pegreffii, while others resulted in 99% diagnosis between A. berlandi and the other two species. Simple sequence repeat (SSR) loci also allowed us to estimate the genetic differentiation of A. berlandi from A. pegreffii (F st ≈ 0.45, Dc = 0.82) and A. simplex (s. s.) (F st ≈ 0.57, Dc = 0.73). The results suggest that SSRs provide a set of candidate markers for population genetics analysis of A. berlandi, as well as for the investigation, through a multi-locus genotyping approach, of possible patterns of hybridisation/introgression events between A. berlandi and the other two Anisakis species in sympatric conditions.

TITLE: Utilité des loci microsatellites pour la caractérisation génétique interspécifique d'Anisakis berlandi (Nematoda, Anisakidae). ABSTRACT: Huit loci microsatellites, récemment développés chez l'espèce Anisakis pegreffii, ont été amplifiés avec succès chez Anisakis berlandi, espèce sœur du complexe A. simplex (s. l.). Ils ont été validés sur des spécimens adultes (n = 46) de l'espèce, récoltés chez deux individus de l'hôte définitif, le globicéphale commun Globicephala melas, des eaux néo-zélandaises. Parmi les huit loci notés, l'un, Anisl 07132, avait des allèles nuls chez A. berlandi et a donc été exclu de l'analyse génétique ultérieure. Deux loci, Anisl 00314 et Anisl 10535, étaient monomorphes. De plus, comme cela a également été détecté précédemment dans les autres espèces du complexe A. simplex (s. l.), le locus Anisl 7 était lié au sexe, montrant une hémizygosité chez les spécimens mâles. Chez A. berlandi, des distributions de fréquences d'allèles, différentielles par rapport à celles précédemment observées chez A. pegreffii et A. simplex (s. s.), ont été trouvées pour certains loci microsatellites. Le locus Anisl 7 a fourni un diagnostic à 100 % entre A. berlandi et A. pegreffii, tandis que d'autres ont abouti à un diagnostic à 99 % entre A. berlandi et les deux autres espèces. Les loci des SSR ont également permis d'estimer la différenciation génétique d'A. berlandi par rapport à A. pegreffii (F st ≈ 0,45, Dc = 0,82) et A. simplex (s. s.) (F st ≈ 0,57, Dc = 0,73). Les résultats suggèrent que les répétitions de séquences simples (SSR) fournissent un ensemble de marqueurs candidats pour l'analyse génétique des populations d'A. berlandi, ainsi que pour l'investigation, dans une approche de génotypage multilocus, des modèles possibles d'hybridation/introgression entre A. berlandi et les deux autres espèces d'Anisakis dans des conditions sympatriques.

Young sex chromosomes in plants and animals.

A major reason for studying plant sex chromosomes is that they may often be 'young' systems. There is considerable evidence for the independent evolution of separate sexes within plant families or genera, in some cases showing that the maximum possible time during which their sex-determining genes have existed must be much shorter than those of several animal taxa. Consequently, their sex-linked regions could either have evolved soon after genetic sex determination arose or considerably later. Plants, therefore, include species with both young and old systems. I review several questions about the evolution of sex-determining systems and sex chromosomes that require studies of young systems, including: the kinds of mutations involved in the transition to unisexual reproduction from hermaphroditism or monoecy (a form of functional hermaphroditism); the times when they arose; and the extent to which the properties of sex-linked regions of genomes reflect responses to new selective situations created by the presence of a sex-determining locus. I also evaluate which questions are best studied in plants, vs other suitable candidate organisms. Studies of young plant systems can help understand general evolutionary processes that are shared with the sex chromosomes of other organisms.

Early Sex-Chromosome Evolution in the Diploid Dioecious Plant Mercurialis annua.

Suppressed recombination allows divergence between homologous sex chromosomes and the functionality of their genes. Here, we reveal patterns of the earliest stages of sex-chromosome evolution in the diploid dioecious herb Mercurialis annua on the basis of cytological analysis, de novo genome assembly and annotation, genetic mapping, exome resequencing of natural populations, and transcriptome analysis. The genome assembly contained 34,105 expressed genes, of which 10,076 were assigned to linkage groups. Genetic mapping and exome resequencing of individuals across the species range both identified the largest linkage group, LG1, as the sex chromosome. Although the sex chromosomes of M. annua are karyotypically homomorphic, we estimate that about one-third of the Y chromosome, containing 568 transcripts and spanning 22.3 cM in the corresponding female map, has ceased recombining. Nevertheless, we found limited evidence for Y-chromosome degeneration in terms of gene loss and pseudogenization, and most X- and Y-linked genes appear to have diverged in the period subsequent to speciation between M. annua and its sister species M. huetii, which shares the same sex-determining region. Taken together, our results suggest that the M. annua Y chromosome has at least two evolutionary strata: a small old stratum shared with M. huetii, and a more recent larger stratum that is probably unique to M. annua and that stopped recombining ∼1 MYA. Patterns of gene expression within the nonrecombining region are consistent with the idea that sexually antagonistic selection may have played a role in favoring suppressed recombination.

Familial digit ratio (2D:4D) associations in a general population sample from Wales.

BACKGROUND: The relative length of the second and fourth fingers (2D:4D) may be a sex-linked correlate of prenatal androgen exposure. However, the nature of the sex-linkage is controversial, with evidence for both X- and Y-linkage of the 2D:4D phenotype. AIMS: To examine transgenerational effects relating to sex-linkage. In addition, assortative mating on 2D:4D was considered, as well as associations between 2D:4D and age and sex. STUDY DESIGN: A family study was conducted. Parents and offspring completed a demographic questionnaire, and digit ratios were calculated from photocopies of participants' hands. SUBJECTS: We recruited and phenotyped 585 individuals attending a cultural festival in Wales. 2D:4D information was available for 47 mother-son dyads, 70 mother-daughter dyads, 31 father-son dyads and 30 father-daughter dyads. OUTCOME MEASURES: Correlations between 2D:4D of parents and children, as well as between mothers and fathers were conducted. 2D:4D was also examined in relation to age and sex. RESULTS AND CONCLUSIONS: There was a sex difference in 2D:4D (males

Rapid Changes in the Sex Linkage of Male Coloration in Introduced Guppy Populations.

Theory predicts that the sex linkage of sexually selected traits can influence the direction and rate of evolution and should itself evolve in response to sex-specific selection. Some studies have found intraspecific differences in sex linkage associated with differences in selection pressures, but we know nothing about how fast these differences can evolve. Here we show that introduced guppy populations showing rapid evolution of male coloration also show rapid changes in sex-linkage patterns. A comparison, using hormonal manipulations in females, of introduced populations of different ages suggests a consistent increase of autosomal or X-linked coloration 2 years after introduction from high- to low-predation environments. Twenty years after introduction, populations already show the same pattern of coloration inheritance typical of natural low-predation populations in similar habitats. These results highlight that the contemporary evolution of sexually selected traits ought to be studied in concert with contemporary changes in linkage relationships.

The Relative Contributions of the X Chromosome and Autosomes to Local Adaptation.

Models of sex chromosome and autosome evolution yield key predictions about the genomic basis of adaptive divergence, and such models have been important in guiding empirical research in comparative genomics and studies of speciation. In addition to the adaptive differentiation that occurs between species over time, selection also favors genetic divergence across geographic space, with subpopulations of single species evolving conspicuous differences in traits involved in adaptation to local environmental conditions. The potential contribution of sex chromosomes (the X or Z) to local adaptation remains unclear, as we currently lack theory that directly links spatial variation in selection to local adaptation of X-linked and autosomal genes. Here, we develop population genetic models that explicitly consider the effects of genetic dominance, effective population size, and sex-specific migration and selection on the relative contributions of X-linked and autosomal genes to local adaptation. We show that X-linked genes should nearly always disproportionately contribute to local adaptation in the presence of gene flow. We also show that considerations of dominance and effective population size-which play pivotal roles in the theory of faster-X adaptation between species-have surprisingly little influence on the relative contribution of the X chromosome to local adaptation. Instead, sex-biased migration is the primary mediator of the strength of spatial large-X effects. Our results yield novel predictions about the role of sex chromosomes in local adaptation. We outline empirical approaches in evolutionary quantitative genetics and genomics that could build upon this new theory.

Rearrangement hotspots in the sex chromosome of the Palearctic black fly Simulium bergi (Diptera, Simuliidae).

An extreme example of nonrandom rearrangements, especially inversion breaks, is described in the polytene chromosomes of the black fly Simulium bergi Rubtsov, 1956 from Armenia and Turkey. A total of 48 rearrangements was discovered, relative to the standard banding sequence for the subgenus Simulium Latreille, 1802. One rearrangement, an inversion (IIS-C) in the short arm of the second chromosome, was fixed. Six (12.5%) of the rearrangements were autosomal polymorphisms, and the remaining 41 (85.4%) were sex linked. More than 40 X- and Y-linked rearrangements, predominantly inversions, were clustered in the long arm of the second chromosome (IIL), representing about 15% of the total complement. The pattern conforms to a nonrandom model of chromosome breakage, perhaps associated with an underlying molecular mechanism.

Plant Sex Chromosomes.

Although individuals in most flowering plant species, and in many haploid plants, have both sex functions, dioecious species-in which individuals have either male or female functions only-are scattered across many taxonomic groups, and many species have genetic sex determination. Among these, some have visibly heteromorphic sex chromosomes, and molecular genetic studies are starting to uncover sex-linked markers in others, showing that they too have fully sex-linked regions that are either too small or are located in chromosomes that are too small to be cytologically detectable from lack of pairing, lack of visible crossovers, or accumulation of heterochromatin. Detailed study is revealing that, like animal sex chromosomes, plant sex-linked regions show evidence for accumulation of repetitive sequences and genetic degeneration. Estimating when recombination stopped confirms the view that many plants have young sex-linked regions, making plants of great interest for studying the timescale of these changes.

Sexual dimorphism in a trophically polymorphic cichlid fish?

Sexual dimorphism in ecologically relevant traits is ubiquitous in animals. However, other types of intraspecific phenotypic divergence, such as trophic polymorphism, are less common. Because linkage to sex should often lead to balancing selection, understanding the association between sex and phenotypic divergence could help explain why particular species show high morphological variability. To determine if sexual dimorphism could be helping to maintain ecomorphological variation in a classic case of intraspecific trophic polymorphism, we examined the association between sex and morphological divergence in the cichlid Herichthys minckleyi. Although H. minckleyi with enlarged molariform teeth on their pharyngeal jaws have been reported to more commonly be male, we did not find an association between sex and pharyngeal morphotype. Sex was associated with divergence in body size (as measured through standard length). But, sex was not associated with any of the other trophic traits examined. However, pharyngeal morphotype did show an association with gut length, gape, and tooth number. Sexual dimorphism is not playing a central role in enhancing trophic diversity within H. minckleyi.

Plant contributions to our understanding of sex chromosome evolution.

A minority of angiosperms have male and female flowers separated in distinct individuals (dioecy), and most dioecious plants do not have cytologically different (heteromorphic) sex chromosomes. Plants nevertheless have several advantages for the study of sex chromosome evolution, as genetic sex determination has evolved repeatedly and is often absent in close relatives. I review sex-determining regions in non-model plant species, which may help us to understand when and how (and, potentially, test hypotheses about why) recombination suppression evolves within young sex chromosomes. I emphasize high-throughput sequencing approaches that are increasingly being applied to plants to test for non-recombining regions. These data are particularly illuminating when combined with sequence data that allow phylogenetic analyses, and estimates of when these regions evolved. Together with comparative genetic mapping, this has revealed that sex-determining loci and sex-linked regions evolved independently in many plant lineages, sometimes in closely related dioecious species, and often within the past few million years. In reviewing recent progress, I suggest areas for future work, such as the use of phylogenies to allow the informed choice of outgroup species suitable for inferring the directions of changes, including testing whether Y chromosome-like regions are undergoing genetic degeneration, a predicted consequence of losing recombination.

Mother-offspring and nest-mate resemblance but no heritability in early-life telomere length in white-throated dippers.

Telomeres are protective DNA-protein complexes located at the ends of eukaryotic chromosomes, whose length has been shown to predict life-history parameters in various species. Although this suggests that telomere length is subject to natural selection, its evolutionary dynamics crucially depends on its heritability. Using pedigree data for a population of white-throated dippers (Cinclus cinclus), we test whether and how variation in early-life relative telomere length (RTL, measured as the number of telomeric repeats relative to a control gene using qPCR) is transmitted across generations. We disentangle the relative effects of genes and environment and test for sex-specific patterns of inheritance. There was strong and significant resemblance among offspring sharing the same nest and offspring of the same cohort. Furthermore, although offspring resemble their mother, and there is some indication for an effect of inbreeding, additive genetic variance and heritability are close to zero. We find no evidence for a role of either maternal imprinting or Z-linked inheritance in generating these patterns, suggesting they are due to non-genetic maternal and common environment effects instead. We conclude that in this wild bird population, environmental factors are the main drivers of variation in early-life RTL, which will severely bias estimates of heritability when not modelled explicitly.

Tebufenozide resistance is associated with sex-linked inheritance in Plutella xylostella.

The diamondback moth (DBM), Plutella xylostella (L.), is a major pest of cruciferous crops. Tebufenozide, a novel nonsteroidal ecdysone agonist, exhibits good efficacy and has played an increasingly important role in the control of Lepidopteran pests in China. For its resistance management, the genetic basis of tebufenozide resistance was studied using a laboratory selected resistant strain of DBM (resistant ratio, RR = 268). A series of crosses with laboratory susceptible and resistant strains revealed that tebufenozide resistance in this pest was partially biased toward female heredity, with a large difference in RR for F1 (RR = 29) and rF1 progeny (RR = 147). The dominance calculated for these 2 cross progeny was -0.788 and 0.09, respectively. Further analysis showed that the susceptible male and female larvae were similar in their sensitivity to tebufenozide, but the resistant female larvae showed significantly higher resistance than the resistant male larvae. The heredity of tebufenozide resistance in DBM might be linked with the W sex chromosome, which suggested that DBM has the ability to develop high levels of resistance to tebufenozide. This is the first report of sex-linked inheritance of tebufenozide resistance in P. xylostella (L.).

Selection and inheritance of sexually dimorphic juvenile plumage coloration.

Sexually dimorphic plumage coloration is widespread in birds and is generally thought to be a result of sexual selection for more ornamented males. Although many studies find an association between coloration and fitness related traits, few of these simultaneously examine selection and inheritance. Theory predicts that sex-linked genetic variation can facilitate the evolution of dimorphism, and some empirical work supports this, but we still know very little about the extent of sex linkage of sexually dimorphic traits. We used a longitudinal study on juvenile Florida scrub-jays (Aphelocoma coerulescens) to estimate strength of selection and autosomal and Z-linked heritability of mean brightness, UV chroma, and hue. Although plumage coloration signals dominance in juveniles, there was no indication that plumage coloration was related to whether or not an individual bred or its lifetime reproductive success. While mean brightness and UV chroma are moderately heritable, hue is not. There was no evidence for sex-linked inheritance of any trait with most of the variation explained by maternal effects. The genetic correlation between the sexes was high and not significantly different from unity. These results indicate that evolution of sexual dimorphism in this species is constrained by low sex-linked heritability and high intersexual genetic correlation.