Evolutionary Genomics of Sexual Dimorphism
My research focuses on understanding the development of phenotypic differences between males and females. I integrate molecular and population genetic tools to study the evolutionary forces and regulatory mechanisms underpinning these sexually dimorphic traits. I also explore how and why sex chromosomes originate and degenerate, and the processes that lead to transitions in sex-determining mechanisms.
I completed my PhD in Evolutionary Genetics at University College London working in Judith Mank’s group, where I continued as a Postdoctoral Researcher at the University of British Columbia. I am currently an EMBO fellow working in Tanja Schwander's lab at the University of Lausanne.
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 combine genomic and transcriptomic data to study the evolution of sex chromosomes and of sex-biased gene expression and their role in sexual dimorphism.
Images: Poecilia picta, blush male (top left), regular male (bottom left), and female (right). Poecilia reticulata, male (right), female (left). Courtesy of Wouter van der Bijl and Jacelyn Shu
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. Read More
Image: Male:female differences in read coverage across the sex chromosomes of Poecilia 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.
Consequences of sex chromosome degeneration
Y chromosome 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. Read More
Image: Evolution of complete dosage compensation in Poecilia 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. Read More
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 transcriptomics data from multiple guppy tissues. Read More
Image: Dimensional reduction and clustering analysis of single-cell transcriptomes from guppy skin. Each dot represents the transcriptome from one cell, with similarly expressed cells clustered together. Cell types more abundant in females are shown in red and those more abundant in males in blue.
The genomic architecture of sex-specific adaptation
An ideal way for studying the molecular signatures of sex-specific selection and sexual conflict is to compare species with different levels of phenotype complexity, such as species with separate sexes and parthenogenetic species. Because parthenogenetic species consist solely of females only the female phenotypes are subject to selection and they are thus free to evolve without potential constraints imposed by simultaneous selection on male phenotypes. I leverage the multiple, independent transitions from sexual to parthenogenetic reproduction that have occurred across Timema stick insects to investigate the evolution of different regulatory mechanisms under sex-specific selection. Using comparative transcriptomic analyses, I identify convergent patterns of gene expression, alternative splicing and gene regulatory networks associated with sex-specific adaptations. I also test how the genomic architecture shifts following the loss of sex and loss of sexual conflicts.
Image: Timema cristinae, male (top) and female (bottom) © Bart Zijlstra / www.bartzijlstra.com
Haploid selection and rates of gene sequence evolution
Most of the studies on the transcriptional basis of sexual dimorphism focus on animal systems, while far fewer plant species in general, and dioecious angiosperms in particular, have been studied in this regard. To explore differences and shared aspects in the evolution of sex-biased gene expression between plants and animals, I analyzed the molecular evolution of sex-biased genes in a dioecious willow species. We found that male-biased genes expressed in pollen grain abundant tissues are unmasked during haploid stages of the life cycle and thus subject to stronger purifying selection to remove deleterious mutations. This process may prevent male-biased genes from evolving faster in plants, in contrast to animals in which selection on the haploid stage is minimal. Read More
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.
For a recent overview of my research, watch my recent talk from the Collège de France Colloquium on The Evolution of Sex Chromosomes and Supergenes:
Goberdhan V, Darolti I, Mank JE, Corral-Lopez A. Experience with mating receptivity cues affects sexual behaviour of male guppies, but not their strength of preference towards receptive females. BioRxiv
Corral-Lopez A, Bloch NI, van der Bijl W, Cortazar-Chinarro M, Szorkovszky A, Kotrschal A, Darolti I, Amcoff M, Buechel SD, Romenskyy M, Kolm N, Mank JE. Functional convergence of genomic and transcriptomic genetic architecture underlying sociability in a live-bearing fish. Nature Ecology and Evolution in press
Darolti I, Fong JLM, Sandkam BA, Metzger DCH, Mank JE (2023) Sex chromosome heteromorphism and the Fast-X effect in poeciliids. Molecular Ecology 32:4599
Fong LJM, Darolti I, Metzger DCH, Morris J, Lin Y, Sandkam BA, Mank JE (2023) Evolutionary history of the Poecilia picta sex chromosomes. Genome Biology and Evolution 15:evad030
Lin Y, Darolti I, van der Bijl W, Morris J, Mank JE (2023) Extensive variation in germline de novo mutations in Poecilia reticulata. Genome research in press
Darolti I, Mank JE (2023) Sex-biased gene expression at single-cell resolution: Cause and consequence of sexual dimorphism. Evolution Letters 7:148
Meunier C*, Darolti I*, Reimegård J, Mank JE, Johannesson H (2022) Nuclear-specific gene expression in heterokaryons of the filamentous ascomycete Neurospora tetrasperma. Proceedings of the Royal Society, B 289:20220971 (* Joint first authors)
Lin Y, Darolti I, Furman BLS, Almeida P, Sandkam BA, Breden F, Wright AE, Mank JE (2022) Gene duplication to the Y chromosome in Trinidadian guppies. Molecular Ecology 31:1853
Darolti I, Mank JE (2022) A bioinformatic toolkit to simultaneously identify sex and sex-linked regions. Molecular Ecology Resources 22:455
Metzger DCH, Sandkam BA, Darolti I, Mank JE (2021) Rapid evolution of complete dosage compensation in Poeciliids. Genome Biology and Evolution 13:evab155
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
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 5:939
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, and for my current postdoctoral fellowship from the European Molecular Biology Organization.