Recurrent allopolyploidization, Y-chromosome introgression and the evolution of sexual systems in the plant genus Mercurialis.

The plant genus Mercurialis includes dioecious, monoecious and androdioecious species (where males coexist with hermaphrodites). Its diversification involved reticulate evolution via hybridization and polyploidization. The Y chromosome of the diploid species Mercurialis annua shows only mild signs of degeneration. We used sequence variation at a Y-linked locus in several species and at multiple autosomal and pseudoautosomal loci to investigate the origin and evolution of the Y chromosome across the genus. Our study provides evidence for further cases of allopolyploid speciation. It also reveals that all lineages with separate sexes (with one possible exception) share the same ancestral Y chromosome. Surprisingly, males in androdioecious populations of hexaploid M. annua carry a Y chromosome that is not derived from either of its two putative progenitor lineages but from a more distantly related perennial dioecious lineage via introgression. These results throw new light on the evolution of sexual systems and polyploidy in Mercurialis and secure it as a promising model for further study of plant sex chromosomes. This article is part of the theme issue 'Sex determination and sex chromosome evolution in land plants'

Evolutionary and developmental dynamics of sex-biased gene expression in common frogs with proto-Y chromosomes.

The patterns of gene expression on highly differentiated sex chromosomes differ drastically from those on autosomes, due to sex-specific patterns of selection and inheritance. As a result, X chromosomes are often enriched in female-biased genes (feminization) and Z chromosomes in male-biased genes (masculinization). However, it is not known how quickly sexualization of gene expression and transcriptional degeneration evolve after sex-chromosome formation. Furthermore, little is known about how sex-biased gene expression varies throughout development. We sample a population of common frogs (Rana temporaria) with limited sex-chromosome differentiation (proto-sex chromosome), leaky genetic sex determination evidenced by the occurrence of XX males, and delayed gonadal development, meaning that XY individuals may first develop ovaries before switching to testes. Using high-throughput RNA sequencing, we investigate the dynamics of gene expression throughout development, spanning from early embryo to froglet stages. Our results show that sex-biased expression affects different genes at different developmental stages and increases during development, reaching highest levels in XX female froglets. Additionally, sex-biased gene expression depends on phenotypic, rather than genotypic sex, with similar expression in XX and XY males; correlates with gene evolutionary rates; and is not localized to the proto-sex chromosome nor near the candidate sex-determining gene Dmrt1. The proto-sex chromosome of common frogs does not show evidence of sexualization of gene expression, nor evidence for a faster rate of evolution. This challenges the notion that sexually antagonistic genes play a central role in the initial stages of sex-chromosome evolution

Tissue Specificity and Dynamics of Sex-Biased Gene Expression in a Common Frog Population with Differentiated, Yet Homomorphic, Sex Chromosomes.

Sex-biased genes are central to the study of sexual selection, sexual antagonism, and sex chromosome evolution. We describe a comprehensive de novo assembled transcriptome in the common frog <i>Rana temporaria</i> based on five developmental stages and three adult tissues from both sexes, obtained from a population with karyotypically homomorphic but genetically differentiated sex chromosomes. This allows the study of sex-biased gene expression throughout development, and its effect on the rate of gene evolution while accounting for pleiotropic expression, which is known to negatively correlate with the evolutionary rate. Overall, sex-biased genes had little overlap among developmental stages and adult tissues. Late developmental stages and gonad tissues had the highest numbers of stage- or tissue-specific genes. We find that pleiotropic gene expression is a better predictor than sex bias for the evolutionary rate of genes, though it often interacts with sex bias. Although genetically differentiated, the sex chromosomes were not enriched in sex-biased genes, possibly due to a very recent arrest of XY recombination. These results extend our understanding of the developmental dynamics, tissue specificity, and genomic localization of sex-biased genes

Size and Content of the Sex-Determining Region of the Y Chromosome in Dioecious <i>Mercurialis annua</i>, a Plant with Homomorphic Sex Chromosomes.

Dioecious plants vary in whether their sex chromosomes are heteromorphic or homomorphic, but even homomorphic sex chromosomes may show divergence between homologues in the non-recombining, sex-determining region (SDR). Very little is known about the SDR of these species, which might represent particularly early stages of sex-chromosome evolution. Here, we assess the size and content of the SDR of the diploid dioecious herb &lt;i&gt;Mercurialis annua&lt;/i&gt; , a species with homomorphic sex chromosomes and mild Y-chromosome degeneration. We used RNA sequencing (RNAseq) to identify new Y-linked markers for &lt;i&gt;M. annua.&lt;/i&gt; Twelve of 24 transcripts showing male-specific expression in a previous experiment could be amplified by polymerase chain reaction (PCR) only from males, and are thus likely to be Y-linked. Analysis of genome-capture data from multiple populations of &lt;i&gt;M. annua&lt;/i&gt; pointed to an additional six male-limited (and thus Y-linked) sequences. We used these markers to identify and sequence 17 sex-linked bacterial artificial chromosomes (BACs), which form 11 groups of non-overlapping sequences, covering a total sequence length of about 1.5 Mb. Content analysis of this region suggests that it is enriched for repeats, has low gene density, and contains few candidate sex-determining genes. The BACs map to a subset of the sex-linked region of the genetic map, which we estimate to be at least 14.5 Mb. This is substantially larger than estimates for other dioecious plants with homomorphic sex chromosomes, both in absolute terms and relative to their genome sizes. Our data provide a rare, high-resolution view of the homomorphic Y chromosome of a dioecious plant

2019 Scholars at Work Conference Program

Program for the 2019 Scholars at Work Conference at Minnesota State University, Mankato on March 29, 2019

The genetic architecture of sexually selected traits in two natural populations of Drosophila montana

The work was supported by the National Environment Research Council (grant NE/E015255/1 to MGR and RKB) and the Academy of Finland (project 132619 to AH).We investigated the genetic architecture of courtship song and cuticular hydrocarbon traits in two phygenetically distinct populations of Drosophila montana. To study natural variation in these two important traits, we analysed within-population crosses among individuals sampled from the wild. Hence, the genetic variation analysed should represent that available for natural and sexual selection to act upon. In contrast to previous between-population crosses in this species, no major quantitative trait loci (QTLs) were detected, perhaps because the between-population QTLs were due to fixed differences between the populations. Partitioning the trait variation to chromosomes suggested a broadly polygenic genetic architecture of within-population variation, although some chromosomes explained more variation in one population compared with the other. Studies of natural variation provide an important contrast to crosses between species or divergent lines, but our analysis highlights recent concerns that segregating variation within populations for important quantitative ecological traits may largely consist of small effect alleles, difficult to detect with studies of moderate power.PostprintPeer reviewe

Genetic analysis of post-mating reproductive barriers in hybridizing European Populus species

Molecular genetic analyses of experimental crosses provide important information on the strength and nature of post-mating barriers to gene exchange between divergent populations, which are topics of great interest to evolutionary geneticists and breeders. Although not a trivial task in long-lived organisms such as trees, experimental interspecific recombinants can sometimes be created through controlled crosses involving natural F₁'s. Here, we used this approach to understand the genetics of post-mating isolation and barriers to introgression in Populus alba and Populus tremula, two ecologically divergent, hybridizing forest trees. We studied 86 interspecific backcross (BC₁) progeny and >350 individuals from natural populations of these species for up to 98 nuclear genetic markers, including microsatellites, indels and single nucleotide polymorphisms, and inferred the origin of the cytoplasm of the cross with plastid DNA. Genetic analysis of the BC₁ revealed extensive segregation distortions on six chromosomes, and >90% of these (12 out of 13) favored P. tremula donor alleles in the heterospecific genomic background. Since selection was documented during early diploid stages of the progeny, this surprising result was attributed to epistasis, cyto-nuclear coadaptation, heterozygote advantage at nuclear loci experiencing introgression or a combination of these. Our results indicate that gene flow across ‘porous’ species barriers affects these poplars and aspens beyond neutral, Mendelian expectations and suggests the mechanisms responsible. Contrary to expectations, the Populus sex determination region is not protected from introgression. Understanding the population dynamics of the Populus sex determination region will require tests based on natural interspecific hybrid zones

Recurrent allopolyploidization, Y-chromosome introgression and the evolution of sexual systems in the plant genus <i>Mercurialis</i>

The plant genus Mercurialis includes dioecious, monoecious and androdioecious species (where males coexist with hermaphrodites). Its diversification involved reticulate evolution via hybridization and polyploidization. The Y chromosome of the diploid species Mercurialis annua shows only mild signs of degeneration. We used sequence variation at a Y-linked locus in several species and at multiple autosomal and pseudoautosomal loci to investigate the origin and evolution of the Y chromosome across the genus. Our study provides evidence for further cases of allopolyploid speciation. It also reveals that all lineages with separate sexes (with one possible exception) share the same ancestral Y chromosome. Surprisingly, males in androdioecious populations of hexaploid M. annua carry a Y chromosome that is not derived from either of its two putative progenitor lineages but from a more distantly related perennial dioecious lineage via introgression. These results throw new light on the evolution of sexual systems and polyploidy in Mercurialis and secure it as a promising model for further study of plant sex chromosomes. This article is part of the theme issue ‘Sex determination and sex chromosome evolution in land plants’.</jats:p

Supplementary Information from Recurrent allopolyploidization, Y-chromosome introgression and the evolution of sexual systems in the plant genus <i>Mercurialis</i>

Supplementary information on samples and PCR markers, supplementary results containing pictures of agarose gels and phylogenetic trees

Copulation duration, but not paternity share, potentially mediates inbreeding avoidance in Drosophila montana

Studying the incidence of inbreeding avoidance is important for understanding the evolution of mating systems, especially in the context of mate choice for genetic compatibility. We investigated whether inbreeding avoidance mechanisms have evolved in the malt fly, Drosophila montana, by measuring mating latency (a measure of male attractiveness), copulation duration, days to remating, offspring production, and the proportion of offspring sired by the first (P1) and second (P2) male to mate in full-sibling and unrelated pairs. SNP markers were used for paternity analysis and for calculating pairwise relatedness values (genotype sharing) between mating pairs. We found 18 % inbreeding depression in egg-to-adult viability, suggesting that mating with close relatives is costly. Copulation duration was shorter between previously mated females and their brothers than with unrelated males. Based on an earlier study, shorter copulation is likely to decrease the number of inbred progeny by decreasing female remating time. However, shorter copulations did not lead to lower paternity (P2) of full-sibling males. Progeny production of double-mated females was lower when the second male was a full-sibling as compared to an unrelated male, but we could not distinguish between inbreeding depression and lower female reproductive effort after mating with a relative. Relatedness estimates based on 34 SNPs did not detect any quantitative effect of relatedness variation on copulation duration and progeny production. We suggest that inbreeding depression has been strong enough to select for inbreeding avoidance mechanisms in our Finnish D. montana population.peerReviewe