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Evolution of Drosophila Buzzatii Wings: Modular Genetic Organization

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Evolution of Drosophila Buzzatii Wings: Modular Genetic Organization bioRxiv preprint doi: https://doi.org/10.1101/2021.06.16.448721; this version posted June 17, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Evolution of Drosophila buzzatii wings: Modular genetic organization, 2 sex-biased integrative selection and intralocus sexual conflict 3 short running title: Evolution of Drosophila buzzatii wings 4 Iglesias PP1†*, Machado FA2†*, Llanes S3, Hasson E3, Soto EM3 5 1 Laboratorio de Genética Evolutiva, Universidad Nacional de Misiones – CONICET, Félix de 6 Azara 1552, N3300LQH, Misiones, Argentina. 7 2 Department of Biological Sciences, Virginia Polytechnic Institute and State University, 8 Blacksburg, United States. 9 3 Instituto de Ecología, Genética y Evolución de Buenos Aires (IEGEBA – CONICET), DEGE, 10 Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, 11 Argentina. 12 †These authors contributed equally to this work. 13 *Corresponding authors; e-mail: [email protected] , [email protected] 14 15 Abstract 16 The Drosophila wing is a structure shared by males and females with the 17 main function of flight. However, in males, wings are also used to produce songs, or 18 visual displays during courtship. Thus, observed changes in wing phenotype depend 19 on the interaction between sex-specific selective pressures and the genetic and 20 ontogenetic restrictions imposed by a common genetic architecture. Here, we 21 investigate these issues by studying how the wing has evolved in twelve populations 22 of Drosophila buzzatii raised in common-garden conditions and using an isofemale 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.16.448721; this version posted June 17, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 23 line design. The between-population divergence shows that sexual dimorphism is 24 greater when sex evolves in different directions. Multivariate Qst-Fst analyses 25 confirm that male wing shape is the target for multiple selective pressures, leading 26 males’ wings to diverge more than females’ wings. While the wing blade and the 27 wing base appear to be valid modules at the genetic (G matrix) and among- 28 population (D matrix) levels, the reconstruction of between-population adaptive 29 landscapes (Ω matrix) shows selection as an integrative force. Also, cross-sex 30 covariances reduced the predicted response to selection in the direction of the 31 extant sexual dimorphism, suggesting that selection had to be intensified in order to 32 circumvent the limitations imposed by G. However, such intensity of selection was 33 not able to break the modularity pattern of the wing. The results obtained here show 34 that the evolution of D. buzzatii wing shape is the product of a complex interplay 35 between ontogenetic constraints and conflicting sexual and natural selections. 36 37 Keywords 38 Adaptive landscapes, Genetic architecture, Intralocus sexual conflict, Morphological 39 integration/modularity, Multivariate selection. 40 41 Introduction 42 Understanding changes in morphological structures requires an integrative 43 approach that also considers constraints upon change. How is morphology 44 produced during development in the first place? Is selection in line with these 45 developmental rules? Does selection differ between the sexes? Morphological 46 integration, selection, and between-sex pleiotropy are key factors generating 47 association among traits at larger scales. An integrated developmental pattern or 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.16.448721; this version posted June 17, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 48 the occurrence of sex-specific selection on homologous structures controlled by 49 common genetic machinery (i.e. intralocus sexual conflict) may constrain the 50 evolutionary trajectories of such structures. It is only after evaluating the relative 51 effect of these factors that morphological changes can be understood in the light of 52 the interaction between constraints and their potential for functional adaptation. 53 The wing of Drosophila is a complex structure involved in different functions 54 such as flight and acoustic or visual communication (Wooton, 1992). For a long time, 55 it has been considered as a developmentally integrated structure that constrains 56 adaptive evolution (Houle, Bolstad, Van der Linde, & Hansen, 2017; Klingenberg, 57 2009; Klingenberg & Zaklan, 2000). While these conclusions are mostly based on 58 the hypothesis that the wing is divided into anterior and posterior (AP) 59 compartments (Klingenberg & Zaklan, 2000), recently Muñoz-Muñoz et al. (2016) 60 showed evidence supporting the compartmentalization of this structure along the 61 proximo-distal (PD) axis, forming two different modules, the wing base and the wing 62 blade. These modules were recognized not only on the phenotypic level but also at 63 the genetic and environmental levels, suggesting that it is possibly a consequence of 64 a modular developmental program. 65 From the wing primary task perspective (i.e. flight), the developmental 66 modules seem to match functional modules: the wing base transmits the forces 67 generated by the flight muscles and the wing blade generates the aerodynamic 68 forces necessary to lift the body (Dudley 2002). Although fly's ability is common to 69 both sexes, sex-biased dispersal has been documented in Drosophila (Begon, 1976; 70 Powell, Dobzhansky, Hook, & Wistrand, 1976; Fontdevila & Carson, 1978; Markow 71 & Castrezana, 2000; Mishra, Tung, Shree Sruti, Srivathsa, & Dey, 2020). An 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.16.448721; this version posted June 17, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 72 asymmetric dispersal of the sexes can exert different selective pressures on wing 73 morphology in each sex, leading to a sex-biased evolution of the modules. 74 Drosophila’s wings are also involved in premating behaviors that markedly 75 differentiate the wing’s function between sexes (Ewing, 1983; Dickson, 2008). 76 Except for a few species (within the Drosophila virilis species group; Satokangas, 77 Liimatainen, & Hoikkala, 1994), only males use wings for acoustic or visual 78 communication. Therefore, if wing morphology influences sound production or 79 visual display, only male wings will be subject to selection. This selection on males 80 can cause the displacement of females from their phenotypic optimum, reducing 81 their fitness. It is well documented that the direction and intensity of selection on 82 courtship song have been found to differ among populations and species according 83 to female preferences (Iglesias & Hasson, 2017; Iglesias et al., 2018a; Klappert, 84 Mazzi, Hoikkala, & Ritchie, 2007). 85 Here, we address these issues by investigating how the wing has evolved in 86 twelve populations of the cactophilic species Drosophila buzzatii raised in common- 87 garden conditions and using an isofemale line design. Only the males of the D. 88 buzzatii species use wings to produce a courtship song (Iglesias & Hasson, 2017; 89 Iglesias et al., 2018a; Iglesias, Soto, Soto, Colines, & Hasson, 2018b), and a previous 90 study has shown a rapid divergence of courtship song parameters among these 91 populations (Iglesias et al., 2018a). Thus, we first investigated whether the wings of 92 males and females are evolving differently among the sampled populations. At 93 present, wing modularity at the genetic level has only been tested in the model 94 species D. melanogaster (but see Soto, Carreira, Soto, & Hasson, 2008); however, D. 95 buzzatii is a cactophilic species distantly related to it. The effect of selection and drift 96 accumulate through time in each evolving lineage and can even change the modular 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.16.448721; this version posted June 17, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 97 pattern in an evolutionary context (Martín-Serra, Figueirido, & Palmqvist, 2020; 98 Melo & Marroig, 2015). Thus, we then tested whether the wing in each sex is 99 organized in two modules along the PD (proximo-distal) or the AP (antero- 100 posterior) axis in D. buzzatii. We test these hypotheses by estimating the posterior 101 distribution of the Among-Population (D) and Additive Genetic (G) within and 102 between sexes covariances from a landmark-based analysis. We also estimated the 103 covariance pattern among peaks on the realized adaptive landscape for these 104 populations (Ω) to evaluate the potential effect of selection in defining between- 105 populations patterns of phenotypic
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