Evolutionary Genomics of Sexual Dimorphism
Female (left) and male (right) flowering willow catkins. Male catkins abundant in pollen (bottom right).
Female (top) and male (bottom) guppies.
Female (left) and male (right) jumping spiders.
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Recent conference and seminar contributionsOrganiser
The evolution of sexual dimorphism
Despite sharing the majority of their genome, males and females of the same species often show a wealth of phenotypic differences, affecting morphology, physiology, behavior and life history, among other traits. I am broadly interested in how sex-specific evolutionary forces shape distinct male and female phenotypes. In some species, the two sexes differ by their sex chromosomes, and sex-limited (Y or W) genes partly explain the observed sexual dimorphism. To a large extent, however, sex differences are encoded by genes that are shared between males and females but that are expressed differently in the two sexes (sex-biased genes). In my research, I integrate genomic and transcriptomic data to study the evolution of sex chromosomes and of sex-biased gene expression and their role in sexual dimorphism.
Image: Illustration of a female and two male Endler's guppy (Poecilia wingei). Courtesy of Clara Lacy.
Diversity of sex chromosome systems
Sex chromosomes have repeatedly evolved across the tree of life. However, the recombination landscape and the rate of divergence of sex chromosomes vary significantly across lineages. A persistent question is why do some sex chromosomes exhibit extensive recombination suppression and degeneration while others remain largely undifferentiated. I address this question by characterizing the structure and conservation of sex chromosome systems across guppies and related species.
Image: Male:female differences in read coverage across the sex chromosomes of P. reticulata, P. wingei and P. picta. Purple regions indicate divergence between the X and the Y chromosomes. The sex chromosomes are largely undifferentiated in P. reticulata and P. wingei, while completely non-recombining and degenerated in P. picta.
Evolutionary consequences of sex chromosome degeneration
Y gene activity decay can have widespread genomic consequences. This process can trigger several evolutionary pressures, including selection for dosage compensation and accelerated rates of evolution for X-linked loci. I integrate analyses of sequence divergence, polymorphism and expression data across poeciliid species to study how variation in the extent of degeneration shapes sex chromosome evolution.
Image: Evolution of complete dosage compensation in P. picta. (LEFT) Density plots of major allele ratio for autosomal (gray) and sex-linked genes (yellow) in males. Most sites exhibit strong allele-specific expression indicative of Y gene activity decay. (RIGHT) Despite the profound Y degeneration, males express their single X chromosome at the same level as the autosomes and the two X copies of females.
Sex-biased gene expression
Sexually dimorphic traits have often been studied in relation to differential regulation of genes present in both sexes, referred to as sex-biased gene expression. Depending on the sex in which they are predominantly expressed, sex-biased genes can be divided into male-biased or female-biased, with genes showing similar expression between the sexes referred to as unbiased. Sex-biased genes are thought to evolve in response to conflicting sex-specific selection over optimal expression. Most of the studies on the transcriptional basis of sexual dimorphism focus on animal systems, while far fewer dioecious plant species have been studied in this regard. To explore differences and shared aspects in the evolution of sex-biased expression between plants and animals, I analyzed the molecular evolution of sex-biased genes in a dioecious willow species.
Image: (LEFT) Hierarchical clustering of gene expression. Each row represents a gene, with highly expressed genes in yellow and lowly expressed genes in black. Male and female leaf samples have very similar gene expression profiles, clustering together. In contrast, male and female catkin reproductive samples are dimorphic in their gene expression patterns. (RIGHT) Catkin samples are abundant in sex-biased genes, while leaves have an unbiased expression profile.
The ontogeny and evolution of sex-biased genes
An important outstanding question in the research of sexual dimorphism remains about the proximal causes of observed sex differences in gene expression. Are sex-biased genes the product of regulatory sex differences within similar cell types? Alternatively, are they a consequence of differences in cell type abundance between males and females due to sex-specific developmental programs? To disentangle between these processes, I am analyzing single-cell RNA sequencing data from multiple guppy tissues.
Image: Dimensional reduction and clustering analysis of single-cell transcriptomes from guppy ovary. Each dot represents the transcriptome from one cell. Cells with similar expression profiles are clustered together.
Lin Y, Darolti I, Furman BLS, Almeida P, Sandkam BA, Breden F, Wright AE, Mank JE (2021) Sexual conflict over survival in Trinidadian guppies. BioRxiv
Metzger DCH, Sandkam BA, Darolti I, Mank JE (2021) Rapid evolution of complete dosage compensation in Poeciliids. Genome Biology and Evolution in press.
Sandkam BA, Almeida P, Darolti I, Furman BLS, van der Bijl W, Morris J, Bourne GR, Breden F, Mank JE (2021) Extreme Y chromosome polymorphism corresponds to five male reproductive morphs. Nature Ecology and Evolution in press.
Almeida P, Sandkam BA, Morris J, Darolti I, Breden F, Mank JE (2021) Divergence and remarkable diversity of the Y chromosome in guppies. Molecular Biology and Evolution 38:619.
Morris J, Darolti I, van der Bijl W, Mank JE (2020) High-resolution characterization of male ornamentation and reevaluation of sex linkage in guppies. Proceedings of the Royal Society of London, B 287:20201677.
Darolti I, Wright AE, Mank JE (2020) Guppy Y chromosome integrity maintained by incomplete recombination suppression. Genome Biology and Evolution 12:965.
Furman BLS, Metzger DCH, Darolti I, Wright AE, Sandkam BA, Almeida P, Shu JJ, Mank JE (2020) Sex chromosome evolution: So many exceptions to the rules. Genome Biology and Evolution 12:750.
Darolti I, Wright AE, Sandkam BA, Morris J, Bloch NI, Farré M, Fuller RC, Bourne GR, Larkin DM, Breden F, Mank JE (2019) Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers. Proceedings of the National Academy of Sciences, USA 116:19031.
Farré M, Li Q, Darolti I, Zhou Y, Damas J, Proskuryakova AA, Kulemzina AI, Chemnick LG, Kim J, Ryder OA, Ma J, Graphodatsky AS, Zhang G, Larkin DM, Lewin HA (2019) An integrated chromosome-scale genome assembly of the Masai giraffe (Giraffa camelopardalis tippelskirchi). GigaScience 8:giz090.
Wright AE, Darolti I, Bloch NI, Oostra V, Sandkam BA, Buechel SD, Kolm N, Breden F, Vicoso B, Mank JE (2019) On the power to detect rare recombination events. Proceedings of the National Academy of Sciences, USA 116:12607.
Morris J, Darolti I, Bloch NI, Wright AE, Mank JE (2018) Shared and species-specific patterns of nascent Y chromosome evolution in two guppy species. Genes 9:238.
Fox G, Darolti I, Hibbitt JD, Preziosi RF, Fitzpatrick JL, Rowntree JK (2018) Bespoke markers for ex-situ conservation: application, analysis and challenges in the assessment of a population of endangered undulate rays. Journal of Zoo and Aquarium Research 6:50.
Darolti I, Wright AE, Pucholt P, Berlin S, Mank JE (2018) Slow evolution of sex-biased genes in the reproductive tissue of the dioecious plant S. viminalis. Molecular Ecology 27:694.
Wright AE, Darolti I, Bloch NI, Oostra V, Sandkam BA, Buechel SD, Kolm N, Breden F, Vicoso B, Mank JE (2017) Convergent recombination suppression suggests a role of sexual conflict in guppy sex chromosome formation. Nature Communications 8:14251.
I am very grateful for my PhD research funding from the Biotechnology and Biological Sciences Research Council through the London Interdisciplinary Doctoral Programme.