Extreme Heterogeneity in Sex Chromosome Differentiation and Dosage Compensation in Livebearers
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Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers Iulia Daroltia,1, Alison E. Wrightb, Benjamin A. Sandkamc, Jake Morrisa, Natasha I. Blochd, Marta Farrée, Rebecca C. Fullerf, Godfrey R. Bourneg, Denis M. Larkinh, Felix Bredeni, and Judith E. Manka,c,j aDepartment of Genetics, Evolution and Environment, University College London, London WC1E 6BT, United Kingdom; bDepartment of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, United Kingdom; cDepartment of Zoology, University of British Columbia, Vancouver, BC V6T 1Z4, Canada; dDepartment of Biomedical Engineering, University of Los Andes, Bogotá 111711, Colombia; eSchool of Biosciences, University of Kent, Canterbury CT2 7NJ, United Kingdom; fDepartment of Animal Biology, University of Illinois at Urbana–Champaign, Urbana, IL 61801; gDepartment of Biology, University of Missouri–St. Louis, St. Louis, MO 63105; hDepartment of Comparative Biomedical Sciences, Royal Veterinary College, London NW1 0TU, United Kingdom; iDepartment of Biological Science, Simon Fraser University, Burnaby, BC V5A 1S6, Canada; and jDepartment of Organismal Biology, Uppsala University, Uppsala 752 36, Sweden Edited by David M. Hillis, The University of Texas at Austin, Austin, TX, and approved August 6, 2019 (received for review April 1, 2019) Once recombination is halted between the X and Y chromosomes, yet profoundly distinct, in others (18). Comparing the structure sex chromosomes begin to differentiate and transition to hetero- and recombination patterns of sex chromosomes between closely morphism. While there is a remarkable variation across clades in related species is a powerful method to determine the forces the degree of sex chromosome divergence, far less is known about shaping sex chromosome evolution over time. the variation in sex chromosome differentiation within clades. Sex chromosome divergence can also lead to differences in X Here, we combined whole-genome and transcriptome sequenc- chromosome gene dose between males and females. Following ing data to characterize the structure and conservation of sex recombination suppression, the Y chromosome undergoes gradual chromosome systems across Poeciliidae, the livebearing clade that degradation of gene activity and content, leading to reduced gene includes guppies. We found that the Poecilia reticulata XY system dose in males (6, 19, 20). Genetic pathways that incorporate both is much older than previously thought, being shared not only with autosomal and sex-linked genes are primarily affected by such its sister species, Poecilia wingei, but also with Poecilia picta, which EVOLUTION diverged roughly 20 million years ago. Despite the shared ances- imbalances in gene dose, with potential severe phenotypic con- try, we uncovered an extreme heterogeneity across these species sequences for the heterogametic sex (21). In some species, this in the proportion of the sex chromosome with suppressed recom- process has led to the evolution of chromosome-level mecha- bination, and the degree of Y chromosome decay. The sex chro- nisms to compensate for the difference in gene dose (22, 23). mosomes in P. reticulata and P. wingei are largely homomorphic, However, the majority of sex chromosome systems are associated with recombination in the former persisting over a substantial fraction. However, the sex chromosomes in P. picta are com- Significance pletely nonrecombining and strikingly heteromorphic. Remark- ably, the profound degradation of the ancestral Y chromosome Morphologically and functionally distinct X and Y chromosomes in P. picta is counterbalanced by the evolution of functional have repeatedly evolved across the tree of life. However, the chromosome-wide dosage compensation in this species, which extent of differentiation between the sex chromosomes varies has not been previously observed in teleost fish. Our results offer substantially across species. As sex chromosomes diverge, the Y important insight into the initial stages of sex chromosome evo- chromosome gene activity decays, leaving genes on the sex lution and dosage compensation. chromosomes reduced to a single functional copy in males. Mechanisms have evolved to compensate for this reduction in Y degeneration | dosage compensation | recombination | poeciliids gene dosage. Here, we perform a comparative analysis of sex chromosome systems across poeciliid species and uncover ex- ex chromosome evolution is characterized by remarkable treme variation in the degree of sex chromosome differentiation Svariation across lineages in the degree of divergence between and Y chromosome degeneration. Additionally, we find evi- the X and Y chromosomes (1, 2). Derived from a pair of ho- dence for a case of chromosome-wide dosage compensation in mologous autosomes, sex chromosomes begin to differentiate as fish. Our findings have important implications for sex chromo- recombination between them is suppressed in the heterogametic some evolution and regulation. sex over the region spanning a newly acquired sex-determining locus (3, 4). The lack of recombination exposes the sex-limited Y Author contributions: I.D. and J.E.M. designed research; I.D., A.E.W., J.M., and N.I.B. per- chromosome to a range of degenerative processes that cause it formed research; I.D., A.E.W., and J.M. analyzed data; B.A.S., R.C.F., G.R.B., F.B., and J.E.M. collected data; G.R.B. provided logistical support in Guyana; M.F. and D.M.L. provided to diverge in structure and function from the corresponding X analysis support; and I.D., A.E.W., B.A.S., J.M., N.I.B., M.F., R.C.F., G.R.B., D.M.L., F.B., and chromosome, which still recombines in females (5, 6). Conse- J.E.M. wrote the paper. quently, the sex chromosomes are expected to eventually transi- The authors declare no conflict of interest. tion from a homomorphic to heteromorphic structure, supported This article is a PNAS Direct Submission. by evidence from many of the old and highly differentiated sys- This open access article is distributed under Creative Commons Attribution License 4.0 tems found in mammals (7, 8), birds (9), Drosophila (5), and (CC BY). snakes (10). Data deposition: DNA-sequencing and RNA-sequencing reads have been deposited at the However, there is a significant heterogeneity among clades, National Center for Biotechnology Information Sequencing Read Archive (BioProject ID and even among species with shared sex chromosome systems, in PRJNA353986 for Poecilia reticulata reads and BioProject ID PRJNA528814 for Poecilia wingei, Poecilia picta, Poecilia latipinna, and Gambusia holbrooki reads) and at the Eu- the spread of the nonrecombining region, and the subsequent ropean Nucleotide Archive (ID PRJEB26489 for P. wingei paired-end DNA-sequencing degree of sex chromosome divergence (11–13). Age does not reads). always reliably correlate with the extent of recombination sup- 1To whom correspondence may be addressed. Email: [email protected]. pression, as the sex chromosomes maintain a largely homomor- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. phic structure over long evolutionary periods in some species 1073/pnas.1905298116/-/DCSupplemental. (12, 14–17), while the 2 sex chromosomes are relatively young, www.pnas.org/cgi/doi/10.1073/pnas.1905298116 PNAS Latest Articles | 1of6 Downloaded by guest on October 1, 2021 with gene-by-gene level mechanisms, whereby dosage-sensitive genes (DNA-seq) with an average of 222 million 150-base pair (bp) are compensated, but overall expression of the X chromosome is paired-end reads (average insert size of 500 bp, resulting in an lower in males compared with females (20, 23, 24). average of 76-fold coverage) and 77.8 million 150-bp mate-pair As opposed to most mammals and birds, the sex chromosomes reads (average insert size of 2 kb, averaging 22-fold coverage) of many fish, lizard, and amphibian species are characterized by per individual. We also generated, on average, 26.6 million 75-bp a lack of heteromorphism, which has usually been attributed to paired-end RNA-seq reads for each individual. processes such as sex chromosome turnover and sex reversal (16, Previous work on the sex chromosomes of these species 25–30). As a result, closely related species from these taxonomic showed evidence for male heterogametic systems in P. wingei groups often have a variety of sex chromosome systems found at (48), P. picta (50), and G. holbrooki (51), and a female hetero- different stages in evolution (27, 31–33). Alternatively, undif- gametic system in P. latipinna (52, 53). For each target species, ferentiated sex chromosomes in anolis lizards, for example, have we built a scaffold-level de novo genome assembly using been found to be the result of long-term conservation of a ho- SOAPdenovo2 (54) (SI Appendix, Table S2). Each assembly was momorphic ancestral system (34). Additionally, global dosage constructed using the reads from the homogametic sex only in compensation has not yet been found in fish, perhaps due to the order to prevent coassembly of X and Y reads. This allowed us to transient nature of the sex chromosome systems and the general later assess patterns of sex chromosome divergence based on lack of heteromorphism in the group. However, incomplete dos- differences between the sexes in read mapping efficiency to the age compensation, through a gene-by-gene regulation mechanism, genome (detailed below). may have evolved in sticklebacks (35, 36), flatfish (37), and rain- To obtain scaffold positional