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Tartan Underlies the Evolution of Drosophila Male Genital Morphology

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Tartan Underlies the Evolution of Drosophila Male Genital Morphology tartan underlies the evolution of Drosophila male genital morphology Joanna F. D. Hagena, Cláudia C. Mendesa,1, Amber Blogga, Alexander Paynea,2, Kentaro M. Tanakaa,3, Pedro Gaspara, Javier Figueras Jimeneza, Maike Kittelmanna, Alistair P. McGregora,b,4, and Maria D. S. Nunesa,b,4 aDepartment of Biological and Medical Sciences, Oxford Brookes University, OX3 0BP Oxford, United Kingdom; and bCentre for Functional Genomics, Oxford Brookes University, OX3 0BP Oxford, United Kingdom Edited by Brian Charlesworth, University of Edinburgh, Edinburgh, United Kingdom, and approved August 5, 2019 (received for review June 10, 2019) Male genital structures are among the most rapidly evolving The claspers are periphallic structures with an essential role in morphological traits and are often the only features that can grasping and proprioception of the female and in securing gen- distinguish closely related species. This process is thought to be ital coupling (12, 22–27). Previously, we found that multiple loci driven by sexual selection and may reinforce species separation. contribute to divergence in clasper size and bristle number be- However, while the genetic bases of many phenotypic differ- tween D. simulans and D. mauritiana (19). Here, we report the ences have been identified, we still lack knowledge about the identification of one of these loci, tartan (trn). In addition, genes underlying evolutionary differences in male genital or- mapping and functional experiments strongly suggest that cis- gans and organ size more generally. The claspers (surstyli) are regulatory changes in this gene underlie differences in clasper periphallic structures that play an important role in copulation in morphology between these two species. insects. Here, we show that divergence in clasper size and bristle number between Drosophila mauritiana and Drosophila simulans Results and Discussion tartan trn is caused by evolutionary changes in ( ), which encodes Previously, we identified two regions on the left arm of chromo- a transmembrane leucine-rich repeat domain protein that medi- some 3 that contribute to differences in clasper size and bristle ates cell–cell interactions and affinity. There are no fixed amino trn D. mauritiana D. simulans number between D. mauritiana and D. simulans (19). Here, we acid differences in between and , EVOLUTION have generated recombinant introgression lines (ILs) between the but differences in the expression of this gene in developing gen- 501 501 italia suggest that cis-regulatory changes in trn underlie the evo- D. mauritiana D1 (Dmau D1) and D. simulans w (Dsim w ) lution of clasper morphology in these species. Finally, analyses of reciprocal hemizygotes that are genetically identical, except for Significance the species from which the functional allele of trn originates, determined that the trn allele of D. mauritiana specifies larger The morphology of male genitalia evolves rapidly, probably claspers with more bristles than the allele of D. simulans.There- driven by sexual selection. However, little is known about the fore, we have identified a gene underlying evolutionary change genes underlying genitalia differences between species. Iden- in the size of a male genital organ, which will help to better tifying these genes is key to understanding how sexual selec- understand not only the rapid diversification of these structures, tion acts to produce rapid phenotypic change. We have found but also the regulation and evolution of organ size more broadly. that the gene tartan underlies differences between male Drosophila mauritiana and Drosophila simulans in the size evolution | development | genetics | Drosophila | genitalia and bristle number of the claspers—genital projections that grasp the female during copulation. Moreover, since tartan he morphology of male genitalia can differ dramatically even encodes a protein that is involved in cell interactions, this may Tbetween very closely related animal species (1). In Drosophila represent an alternative developmental mechanism for mor- mauritiana males, for example, the size, shape, and bristle mor- phological change. Therefore, our study provides insights into phology of the claspers (surstyli), posterior lobes (epandrial posterior the genetic and developmental bases for the rapid evolution of lobes), and anal plates (cerci) are strikingly different from those male genitalia and organ size more generally. of its sister species Drosophila simulans and Drosophila sechellia Author contributions: J.F.D.H., P.G., A.P.M., and M.D.S.N. designed research; J.F.D.H., (Fig. 1). Moreover, these differences have evolved in only the C.C.M., A.B., A.P., K.M.T., J.F.J., M.K., and M.D.S.N. performed research; J.F.D.H., C.C.M., last 240,000 y since these species last shared a common ancestor A.P., K.M.T., and M.D.S.N. analyzed data; and J.F.D.H., A.P.M., and M.D.S.N. wrote (2) (Fig. 1A). the paper. As in other animal groups (1, 3–5), interspecific differences in The authors declare no conflict of interest. the morphology of genital structures are thought to have been This article is a PNAS Direct Submission. driven by sexual selection (6). However, the mechanisms [female This open access article is distributed under Creative Commons Attribution-NonCommercial- choice, sperm competition, or sexual antagonism (5)], and their NoDerivatives License 4.0 (CC BY-NC-ND). contribution to reproductive isolation between populations and Data deposition: Raw fastq files for the RNA sequencing data reported in this paper have species, have been difficult to address and resolve theoretically been deposited at DNA Data Bank of Japan under accession nos. DRA006755 and (7–9) and experimentally (10, 11). Genetic manipulation of the DRA006758 for D. mauritiana and D. simulans, respectively. 1 evolved loci would allow us to test directly the effect of male Present address: Department of Physiology, Anatomy and Genetics, University of Oxford, OX1 3QX Oxford, United Kingdom. genital divergence on mating behavior and reproductive fitness 2Present address: School of Life Sciences, University of Nottingham, NG7 2UH Notting- and, therefore, facilitate the empirical study of these questions ham, United Kingdom. (12, 13). Although quantitative mapping studies of morphologi- 3Present address: Department of Biological Sciences, Tokyo Metropolitan University, 192- cal differences in male genitalia between species of the D. simulans 0397 Hachioji, Japan. – clade were first carried out more than three decades ago (14 21), 4To whom correspondence may be addressed. Email: [email protected] or the genetic bases of male genital divergence between these species [email protected]. has remained elusive. This is due, at least in part, to the large This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. number of loci found to contribute to variation in size and shape 1073/pnas.1909829116/-/DCSupplemental. of these structures (18, 19, 21). www.pnas.org/cgi/doi/10.1073/pnas.1909829116 PNAS Latest Articles | 1of6 Downloaded by guest on September 26, 2021 on the posterior lobes consistent with region C2 only affecting the claspers (Dataset S4). trn encodes a leucine-rich repeat transmembrane protein (28, 30, 32, 33, 35, 36), and it is thought that its main function is to confer differences in affinity between cells and mediate their correct allocation to compartments in developing tissues such as the nervous system, trachea, eyes, wings, and legs (28, 30, 32, 35, 37, 38). Intriguingly, changes in trn expression can affect the allocation of cells between compartments, cause misspecification of compartmental boundaries, and even result in invasive movements of cells across such boundaries (33, 35, 38). Our RNA-Seq data indicates that trn is more highly expressed in D. simulans during early terminalia development but is sub- sequently up-regulated in D. mauritiana at a later stage (Dataset S3). However, these data correspond to the sum of all of the expression domains of trn throughout the terminalia at each of these stages and may conceal more subtle localized expression differences between these species in specific tissues like the de- veloping claspers. Therefore, we investigated the spatial pattern of trn expression throughout terminalia development using 501 Fig. 1. Divergence in periphallic structures in the D. simulans clade and its mRNA in situ hybridization (ISH) in Dmau D1 and Dsim w relationship to the outgroup D. melanogaster (2). (A) Schematic represen- (Fig. 3 A–C and SI Appendix, Fig. S3). Concomitantly, we ob- tation of the male analia and external genitalia (posterior view). Posterior served a 4-h difference in the timing of terminalia development lobes are illustrated as dissected away on the right-hand side, in order to between the two strains used (Fig. 3 A–C and SI Appendix, Fig. facilitate visualization of the claspers (outlined in orange), which are typi- S3). We found that during early pupal stages trn is more highly cally covered by the posterior lobes. While the shape and size of the pos- expressed in Dsim w501 compared to Dmau D1 at the center of terior lobes is species-specific, the claspers and anal plates are very similar between D. simulans and D. sechellia, which are smaller and have less bristles the terminalia, from where the internal genital structures will than those of D. mauritiana and D. melanogaster. In addition, the clasper develop, which may explain the overall higher expression of trn in bristles of D. mauritiana are shorter and thicker than those of the other D. simulans at 30 h after puparium formation (hAPF) according three species (19, 20, 48). (B–E) Scanning electron micrographs of external to the RNA-Seq data (Fig. 3 A and B and Dataset S3). However, male genitalia (B and C) and dissected claspers (D and E)ofDmau D1 and during later stages, the expression of trn is detected in a wider 501 Dsim w , respectively. (Scale bars, 50 μm.) domain and persists for longer at the base of the developing claspers of Dmau D1 compared to Dsim w501 (Fig.
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