ZZ Top: faster and more adaptive Z chromosome evolution in two Lepidoptera

The rate of divergence for Z or X chromosomes is theoretically predicted to be greater than autosomes, but the possible explanations for this pattern vary, as do empirical results from diverse taxa. Even among moths and butterflies (Lepidoptera), which generally share a single-origin Z chromosome, the handful of available studies give mixed support for faster or more adaptive evolution of the Z chromosome, depending on the species assayed. Here, we examine the molecular evolution of Z chromosomes in two additional lepidopteran species: the Carolina sphinx moth and the monarch butterfly, the latter of which possesses a recent chromosomal fusion yielding a segment of newly Z-linked DNA. We find evidence for both faster and more adaptive Z chromosome evolution in both species, though this effect is strongest in the neo-Z portion of the monarch sex chromosome. The neo-Z is less male-biased than expected of a Z chromosome, and unbiased and female-biased genes drive the signal for adaptive evolution here. Together these results suggest that male-biased gene accumulation and haploid selection have opposing effects on long-term rates of adaptation and may help explain the discrepancies in previous findings as well as the repeated evolution of neo-sex chromosomes in Lepidoptera.

Loss of genetic variation in the two-locus multiallelic haploid model

In the evolutionary biology literature, it is generally assumed that in deterministic haploid selection models, in the absence of variation-generating mechanisms such as mutation, no polymorphic equilibrium can be stable. However, results corroborating this claim are scarce and almost always depend upon additional assumptions. Using ideas from game theory, we establish a condition on the fitness parameters of haplotypes formed by two loci such that a monomorphism is a global attractor. Further, we show that no isolated equilibrium exists, at which an unequal number of alleles from two loci is present. Under the assumption of convergence of trajectories to equilirium points, we settle the two-locus three-allele case for a fitness scheme formally equivalent to the classical symmetric viability model.

Haploid induction in tropical supersweet corn and ploidy determination at the seedling stage

The objective of this work was to determine the possibility of haploid induction in tropical supersweet corn (Zea mays L. var. saccharata) using a maternal inducer, as well as to identify alternative methods for haploid selection. A single-cross hybrid of field corn and 11 tropical supersweet corn populations were crossed with the haploid inducer. The haploids were pre-selected using the R1-navajo marker and were differentiated into haploids or false positives at the V2-V3 stage, based on the color of the first leaf sheath and on the length of stomata guard cells. The obtained results are indicative of the possibility of inducing maternal haploids in populations of tropical supersweet corn. However, a large number of false-positive haploids were incorrectly selected by the R1-navajo marker. The color of the first leaf sheath was efficient for haploid identification in supersweet corn populations, and the method based on stomata morphometry can be used when there is no color distinction on the first leaf sheath.

Haploid Selection in “Diploid” Organisms

Evolutionary rates and strength of selection differ markedly between haploid and diploid genomes. Any genes expressed in a haploid state will be directly exposed to selection, whereas alleles in a diploid state may be partially or fully masked by a homologous allele. This difference may shape key evolutionary processes, including rates of adaptation and inbreeding depression, but also the evolution of sex chromosomes, heterochiasmy, and stable sex ratio biases. All diploid organisms carry haploid genomes, most notably the haploid genomes in gametes produced by every sexually reproducing eukaryote. Furthermore, haploid expression occurs in genes with monoallelic expression, in sex chromosomes, and in organelles, such as mitochondria and plastids. A comparison of evolutionary rates among these haploid genomes reveals striking parallels. Evidence suggests that haploid selection has the potential to shape evolution in predominantly diploid organisms, and taking advantage of the rapidly developing technologies, we are now in the position to quantify the importance of such selection on haploid genomes.

Differential sperm motility mediates the sex ratio drive shaping mouse sex chromosome evolution

SummaryThe search for morphological or physiological differences between X- and Y-bearing mammalian sperm has provoked controversy for decades. Many potential differences have been proposed, but none validated, while accumulating understanding of syncytial sperm development has cast doubt on whether such differences are possible even in principle. We present the first ever mammalian experimental model to trace a direct link from a measurable physiological difference between X- and Y-bearing sperm to the resulting skewed sex ratio. We show that in mice with deletions on chromosome Yq, birth sex ratio distortion is due to a relatively greater motility of X-bearing sperm, and not to any aspect of sperm/egg interaction. Moreover, the morphological distortion caused by Yq deletion is more severe in Y-bearing sperm, providing a potential hydrodynamic basis for the altered motility. This reinforces a growing body of work indicating that sperm haploid selection is an important and underappreciated evolutionary force.

The effects of haploid selection on Y chromosome evolution in two closely related dioecious plants

The evolution of sex chromosomes is usually considered to be driven by sexually antagonistic selection in the diploid phase. However, selection during the haploid gametic phase of the lifecycle has recently received theoretical attention as possibly playing a central role in sex chromosome evolution, especially in plants where gene expression in the haploid phase is extensive. In particular, male-specific haploid selection might favour the linkage of pollen beneficial alleles to male sex determining regions on incipient Y chromosomes. This linkage might then allow such alleles to further specialise for the haploid phase. Purifying haploid selection is also expected to slow the degeneration of Y-linked genes expressed in the haploid phase. Here, we examine the evolution of gene expression in flower buds and pollen of two species of Rumex to test for signatures of haploid selection acting during plant sex chromosome evolution. We find that genes with high ancestral pollen expression bias occur more often on sex chromosomes than autosomes and that genes on the Y chromosome are more likely to become enriched for pollen expression bias. We also find that genes with low expression in pollen are more likely to be lost from the Y chromosome. Our results suggest that sex-specific haploid selection during the gametophytic stage of the lifecycle may be a major contributor to several features of plant sex chromosome evolution.

Haploid selection, sex ratio bias, and transitions between sex-determining systems

Sex determination is remarkably dynamic; many taxa display shifts in the location of sex-determining loci or the evolution of entirely new sex-determining systems. Predominant theories for why we observe such transitions generally conclude that novel sex-determining systems are favoured by selection if they equalise the sex ratio or increase linkage with a locus that experiences different selection in males vs. females. We use population genetic models to extend these theories in two ways: (1) We consider the dynamics of loci very tightly linked to the ancestral sex-determining loci, e.g., within the non-recombining region of the ancestral sex chromosomes. Variation at such loci can favour the spread of new sex-determining systems in which the heterogametic sex changes (XY to ZW or ZW to XY) and the new sex-determining region is less closely linked (or even unlinked) to the locus under selection. (2) We consider selection upon haploid genotypes either during gametic competition (e.g., pollen competition) or meiosis (i.e., non-Mendelian segregation), which can cause the zygotic sex ratio to become biased. Haploid selection can drive transitions between sex-determining systems without requiring selection to act differently in diploid males vs. females. With haploid selection, we find that transitions between male and female heterogamety can evolve where linkage with the sex-determining locus is either strengthened or weakened. Furthermore, we find that sex-ratio biases may increase or decrease with the spread of new sex chromosomes, which implies that transitions between sex-determining systems cannot be simply predicted by selection to equalise the sex ratio. In fact, under many conditions, we find that transitions in sex determination are favoured equally strongly in cases where the sex ratio bias increases or decreases. Overall, our models predict that sex determination systems should be highly dynamic, particularly when haploid selection is present, consistent with the evolutionary lability of this trait in many taxa.Author summarySystems of sex determination are strikingly diverse and labile in many clades. This poses the question: what drives transitions between sex-determining systems? Here, we use models to derive conditions under which new sex-determining systems spread. Prevailing views suggest that new sex-determining systems are favoured when they equalize the sex ratio and/or when they are more closely linked to genes that experience differential selection in males and females. Our models include selection upon haploid genotypes (meiotic drive or gametic competition), which biases the sex-ratio and occurs differently in male and female gametes. Surprisingly, we find the two forces (selection to equalize the sex ratio and the benefits of hitchhiking alongside driven alleles that distort the sex ratio) will often be equally strong, and thus neither is sufficient to explain the spread of new sex-determining systems in every case. We also find that new sex-determining alleles can spread despite being less closely linked to selected loci as long as initial linkage is tight or haploid selection is present. Our models therefore predict that loci in previously unexpected genomic locations and/or experiencing various types of selection (including haploid selection) can now be implicated as drivers of transitions between sex-determining systems.