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Differential Rates of Male Genital Evolution in Sibling Species of Drosophila

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Abstract

Genital morphology in animals with internal fertilization is considered to be among the fastest evolving traits. Sexual selection is often proposed as the main driver of genital diversification but the exact selection mechanisms involved are usually unclear. In addition, the mechanisms operating may differ even between pairs of sibling species. We investigated patterns of male genital variation within and between natural populations of the cactophilic fly Drosophila koepferae ranging its entire geographic distribution and compared them with those previously observed in its sibling species, D. buzzatii. Using both mtDNA and nDNA markers we found that genital shape variation in D. koepferae is more restricted than expected for neutral evolution, suggesting the predominance of stabilizing selection. We also detected dissimilar patterns of divergence between populations of D. koepferae that were allopatric and sympatric with D. buzzatii. The constrained evolution inferred for D. koepferae’s genitalia clearly contrasts with the rapid divergence and higher morphological disparity observed in the populations of D. buzzatii. Finally, different possible scenarios of male genital evolution in each species and within the radiation of D. buzzatii cluster are discussed.

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Fig. 1

(modified from Soto et al. 2007); b aedeagus of the seven recognized species of the Drosophila buzzatii cluster

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References

  • Anderson, C. M., & Langerhans, R. B. (2015). Origins of female genital diversity: Predation risk and lock-and-key explain rapid divergence during an adaptive radiation. Evolution, 69, 2452–2467.

    Article  PubMed  Google Scholar 

  • Anderson, M. J. (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26, 32–46.

    Google Scholar 

  • Arnqvist, G. (1997). The evolution of animal genitalia: Distinguishing between hypotheses by single species studies. Biological Journal of the Linnean Society, 60, 365–379.

    Article  Google Scholar 

  • Arnqvist, G. (1998). Comparative evidence for the evolution of genitalia by sexual selection. Nature, 393(6687), 784–786.

    Article  CAS  Google Scholar 

  • Bonhomme, V., Picq, S., Gaucherel, C., & Claude, J. (2014). Momocs: Outline analysis using R. Journal of Statistical Software, 56, 1–24.

    Article  Google Scholar 

  • Brennan, P. L. R., & Prum, R. O. (2015). Mechanism and evidence of genital coevolution: The roles of natural selection, mate choice, and sexual conflict. Cold Spring Harbor Perspectives in Biology, 7, a017749.

    Article  PubMed  PubMed Central  Google Scholar 

  • Brommer, J. E. (2011). Whither PST? On the approximation of QST by PST in conservation and evolutionary biology. Journal of Evolutionary Biology, 24, 1160–1168.

    Article  CAS  PubMed  Google Scholar 

  • Carreira, V. P., Soto, I. M., Hasson, E., & Fanara, J. J. (2006). Patterns of variation in wing morphology in the cactophilic Drosophila buzzatii and its sibling D. koepferae. Journal of Evolutionary Biology, 9, 1275–1282.

    Article  Google Scholar 

  • Cordero, C., & Eberhard, W. G. (2005). Interaction between sexually antagonistic selection and mate choice in the evolution of female responses to male traits. Evolutionary Ecology, 19, 111–122.

    Article  Google Scholar 

  • De Panis, D., Padró, J., Furió-Tarí, P., Tarazona, S., Soto, I. M., Carmona, M., Conesa, P. A., & Hasson, E. (2016). Transcriptome modulation during host shift is driven by secondary metabolites in desert Drosophila. Molecular Ecology, 25(18), 4534–4550.

    Article  PubMed  Google Scholar 

  • Dommergues, C. H., Dommergues, J. L., & Verrecchia, E. P. (2007). The discrete cosine transform, a Fourier-related method for morphometric analysis of open contours. Mathematical Geology, 39, 749–763.

    Article  CAS  Google Scholar 

  • Dufour, L. (1844). Anatomie générale des Diptères. Annales des Sciences Naturelles, 1, 244–264.

    Google Scholar 

  • Eberhard, W. G. (1985). Sexual selection and animal genitalia. Cambridge: Harvard University Press.

    Book  Google Scholar 

  • Eberhard, W. G. (1993). Evaluating models of sexual selection: Genitalia as a test case. The American Naturalist, 142, 564–571.

    Article  CAS  PubMed  Google Scholar 

  • Eberhard, W. G. (2010). Evolution of genitalia: Theories, evidence, and new directions. Genetica, 138, 5–18.

    Article  PubMed  Google Scholar 

  • Excoffier, L. (2009). Arlequin Ver 3.5. An integrated software package for population genetics data analysis. Bern: Swiss Institute of Bioinformatics, Universitat Bern.

    Google Scholar 

  • Fanara, J. J., Folguera, G., Iriarte, P. F., Mensch, J., & Hasson, E. (2006). Genotype by environment interactions in viability and developmental time in populations of cactophilic Drosophila. Journal of Evolutionary Biology, 19, 900–908.

    Article  CAS  PubMed  Google Scholar 

  • Fanara, J. J., Fontdevila, A., & Hasson, E. (1999). Oviposition preference and life history traits in cactophilic Drosophila koepferae and D. buzzatii in association with their natural hosts. Evolutionary Ecology, 13, 173–190.

    Article  Google Scholar 

  • Foote, M. (1993). Contributions of individual taxa to overall morphological disparity. Paleobiology, 19, 403–419.

    Article  Google Scholar 

  • Foote, M. (1997). The evolution of morphological diversity. Annual Review of Ecology and Systematics, 28, 129–152.

    Article  Google Scholar 

  • Fu, Y. (1997). Statistical test of neutrality of mutations against population growth hitchhiking and background selection. Genetics, 147, 915–925.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garnier, S., Magniez-Jannin, F., Rasplus, J. Y., & Alibert, P. (2005). When morphometry meets genetics: Inferring the phylogeography of Carabus solieri using Fourier analyses of pronotum and male genitalia. Journal of Evolutionary Biology, 18, 269–280.

    Article  CAS  PubMed  Google Scholar 

  • Gower, J. C. (1975). Generalized procrustes analysis. Psychometrika, 40, 33–51.

    Article  Google Scholar 

  • Hankison, S. J., & Ptacek, M. B. (2008). Geographical variation of genetic and phenotypic traits in the Mexican sailfin mollies, Poecilia velifera and P. petenensis. Molecular Ecology, 17, 2219–2233.

    Article  CAS  PubMed  Google Scholar 

  • Hosken, D. J., & Stockley, P. (2004). Sexual selection and genital evolution. Trends in Ecology and Evolution, 19, 8793.

    Article  Google Scholar 

  • House, C. M., Lewis, Z., Hodgson, D. J., Wedell, N., Sharma, M. D., Hunt, J., & Hosken, D. J. (2013). Sexual and natural selection both influence male genital evolution. PLoS ONE, 8, e63807. https://doi.org/10.1371/journal.pone.0063807.

    Article  PubMed  PubMed Central  Google Scholar 

  • House, C. M., & Simmons, L. W. (2003). Genital morphology and fertilization success in the dung beetle Onthophagus taurus: An example of sexually selected male genitalia. Proceedings: Biological Sciences, 27, 447–455.

    Google Scholar 

  • Hurtado, J., Iglesias, P. P., Lipko, P., & Hasson, E. (2013). Multiple paternity and sperm competition in the sibling species Drosophila buzzatii and Drosophila koepferae. Molecular Ecology, 22(19), 5016–5026.

    Article  CAS  PubMed  Google Scholar 

  • Jackson, D. A. (1993). Stopping rules in principal components analysis: A comparison of heuristical and statistical approaches. Ecology, 74(8), 2204–2214.

    Article  Google Scholar 

  • Kamimura, Y. (2012). Correlated evolutionary changes in Drosophila female genitalia reduce the possible infection risk caused by male copulatory wounding. Behavioral Ecology and Sociobiology, 66, 1107–1114.

    Article  Google Scholar 

  • Leinonen, T., Cano, J. M., Mäkinen, H., & Merilä, J. (2006). Contrasting patterns of body shape and neutral genetic divergence in marine and lake populations of threespine sticklebacks. Journal of Evolutionary Biology, 19, 1803–1812.

    Article  CAS  PubMed  Google Scholar 

  • Leinonen, T., Scott McCairns, R. J., O’Hara, R. B., & Merilä, J. (2013). QST – FST comparisons: Evolutionary and ecological insights from genomic heterogenity. Nature, 14, 179–190.

    CAS  Google Scholar 

  • Lipko, P. (2013). Qué historias nos cuentan el ADN mitocondrial y los microsatélites sobre la estructura poblacional de Drosophila koepferae y su especie hermana Drosophila buzzatii en Argentina? Doctoral dissertation. Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires. http://digital.bl.fcen.uba.ar/Download/Tesis/Tesis_5434_Lipko.pdf.

  • Manfrin, M. H., De Brito, R. O. A., & Sene, F. M. (2001). Systematics and evolution of the Drosophila buzzatii (Diptera: Drosophilidae) cluster using mtDNA. Annals of the Entomological Society of America, 94, 334–346.

    Article  Google Scholar 

  • Manfrin, M. H., & Sene, F. M. (2006). Cactophilic Drosophila in South America: A model for evolutionary studies. Genetica, 126, 57–75.

    Article  PubMed  Google Scholar 

  • Masly, J. P. (2012). 170 Years of “Lock-and-Key”: Genital morphology and reproductive isolation. International Journal of Evolutionary Biology, 2012, 247352. https://doi.org/10.1155/2012/247352.

    Article  PubMed  Google Scholar 

  • Mayr, E. (1963). Animal species and evolution. Cambridge, MA: Harvard University Press.

    Book  Google Scholar 

  • McArdle, B. H., & Anderson, M. J. (2001). Fitting multivariate models to community data: A comment on distance-based redundancy analysis. Ecology, 82, 290–297.

    Article  Google Scholar 

  • McPeek, M. A., Shen, L., Torrey, J. Z., & Farid, H. (2008). The tempo and mode of three-dimensional morphological evolution in male reproductive structures. The American Naturalist, 171, 158–178.

    Article  Google Scholar 

  • Naveira, H., & Fontdevila, A. (1986). The evolutionary history of Drosophila buzzatii. XII. The genetic basis of sterility in hybrids between and its sibling from Argentina. Genetics, 114, 841–857.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oksanen, J. F., Blanchet, G., Friendly, F., Kindt, R., Legendre, P., McGlinn, D., et al. (2017). Vegan: Community Ecology Package.

  • Oliveira, D. C. S. G., Almeida, F. C., O’ Grady, P. M., Armella, M. A., De Salle, R., & Etges, W. J. (2012). Monophyly, divergence times, and evolution of host plant use inferred from a revised phylogeny of the Drosophila repleta species group. Molecular Phylogenetics and Evolution, 64, 533–544.

    Article  PubMed  Google Scholar 

  • Piccinali, R., Aguadé, M., & Hasson, E. (2004). Comparative molecular population genetics of the Xdh locus in the cactophilic sibling species Drosophila buzzatii and D. koepferae. Molecular Biology and Evolution, 21, 141–152.

    Article  CAS  PubMed  Google Scholar 

  • Pujol, B., Wilson, A. J., Ross, R. I. C., & Pannell, J. R. (2008). Are QST—FST comparisons for natural populations meaningful? Molecular Ecology, 17, 4782–4785.

    Article  CAS  PubMed  Google Scholar 

  • R Core Team. (2016). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. http://www.R-project.org/.

  • Raeymaekers, J. A. M., Van Houdt, J. K. J., Larmuseau, M. H. D., Geldof, S., & Volckaert, F. A. M. (2007). Divergent selection as revealed by PST and QTL-based FST in three-spined stickleback (Gasterosteus aculeatus) populations along a coastal-inland gradient. Molecular Ecology, 16, 891–905.

    Article  PubMed  Google Scholar 

  • Richmond, M. P., Johnson, S., & Markov, T. A. (2012). Evolution of reproductive morphology among recently diverged taxa in the Drosophila mojavensis species cluster. Ecology and Evolution, 2, 397–408.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rogers, A. R., & Harpending, H. (1992). Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution, 9, 552–569.

    CAS  PubMed  Google Scholar 

  • Rousset, F. (1997). Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics, 145, 1219–1228.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rowe, L., & Arnqvist, G. (2012). Sexual selection and the evolution of genital shape and complexity in water striders. Evolution, 66, 40–54.

    Article  PubMed  Google Scholar 

  • Shapiro, A. M., & Porter, A. H. (1989). The lock-and-key hypothesis: Evolutionary and biosystematic interpretation of insect genitalia. Annual Review of Entomology, 34, 231–245.

    Article  Google Scholar 

  • Simmons, L. W. (2013). Sexual selection and genital evolution. Australian Journal of Entomology, 53, 1–17.

    Google Scholar 

  • Simmons, L. W., House, C. M., Hunt, J., & Garcia-Gonzalez, F. (2009). Evolutionary response to sexual selection in male genital morphology. Current Biology, 19, 1442–1446.

    Article  CAS  PubMed  Google Scholar 

  • Soto, E. M., Goenaga, J., Hurtado, J. P., & Hasson, E. (2012). Oviposition and performance in natural hosts in cactophilic Drosophila. Evolutionary Ecology, 26(4), 975–990.

    Article  Google Scholar 

  • Soto, I. M. (2012). Aedeagal divergence in sympatric populations of two sibling species of cactophilic Drosophila (Diptera: Drosophilidae): Evidence of character displacement? Neotropical Entomology, 41, 207–213.

    Article  CAS  PubMed  Google Scholar 

  • Soto, I. M., Carreira, V. P., Corio, C., Padró, J., Soto, E. M., & Hasson, E. (2014). Differences in tolerance to host cactus alkaloids in Drosophila koepferae and D. buzzatii. PLoS ONE, 9(2), e88370. https://doi.org/10.1371/journal.pone.0088370.

    Article  PubMed  PubMed Central  Google Scholar 

  • Soto, I. M., Carreira, V. P., Fanara, J. J., & Hasson, E. (2007). Evolution of male genitalia: Environmental and genetic factors affecting genital morphology in sibling Drosophila species and their hybrids. BMC Evolutionary Biology, 7, 77.

    Article  PubMed  PubMed Central  Google Scholar 

  • Soto, I. M., Carreira, V. P., Soto, E. M., & Hasson, E. (2008b). Wing morphology and fluctuating asymmetry are dependent of the host plant in cactophilic Drosophila. Journal of Evolutionary Biology, 21(2), 598–609.

    Article  CAS  PubMed  Google Scholar 

  • Soto, I. M., Carreira, V. P., Soto, E. M., Marquez, F., Lipko, P., & Hasson, E. (2013). Rapid divergent evolution of male genitalia among populations of Drosophila buzzatii. Evolutionary Biology, 40, 395–407.

    Article  Google Scholar 

  • Soto, I. M., Manfrin, M. H., & Hasson, E. (2008a). Host-dependent phenotypic plasticity of male genital morphology in cactophilic Drosophila. Journal of Zoological Systematics and Evolutionary Research, 46(4), 368–373.

    Article  Google Scholar 

  • Spitze, K. (1993). Population structure in Daphnia obtusa: Quantitative genetic and allozyme variation. Genetics, 135, 367–374.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tabachnick, B. G., & Fidell, L. S. (2007). Using multivariate statistics (5th ed.). Boston, MA: Pearson International.

    Google Scholar 

  • Tajima, F. (1989). Stastical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585–595.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vilela, C. R. (1983). A revision of the Drosophila repleta species group (Diptera: Drosophilidae). Revista Brasileira de Entomologia, 27, 1–114.

    Google Scholar 

  • Wojcieszek, J. M., & Simmons, L. W. (2012). Evidence for stabilizing selection and slow divergent evolution of males genitalia in a millipede (Antichiropus variabilis). Evolution, 66, 1138–1153.

    Article  PubMed  Google Scholar 

  • Wojcieszek, J. M., & Simmons, L. W. (2013). Divergence in genital morphology may contribute to mechanical reproductive isolation in a millipede. Ecology and Evolution, 3, 334–343.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wright, S. (1951). The genetical structure of populations. Annals of Eugenics, 15, 323–354.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the National Research Council of Argentina (CONICET – PIP 112201500100423CO) and by the National Agency for Scientific and Technological Promotion (PICT 1506–2013) and University of Buenos Aires grants (UBACyT GF2013-2016) with funds granted to IMS. MIS is recipient of postgraduate scholarships from Universidad de Buenos Aires. PMC and PPI are recipients of postgraduate scholarships from CONICET. EMS and IMS are members of Carrera del Investigador Científico (CONICET). Special thanks to Paula Lipko for the assistance with FST calculations and sequence data and to Maite Mascaró Miquela Jauregui and Fernando Nuno Simoes Dias Marques for their kind assistance during drafting of the manuscript.

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  1. Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina

    Manuel I. Stefanini, Patricia P. Iglesias, Eduardo M. Soto & Ignacio M. Soto

  2. Instituto de Ecología, Genética y Evolución de Buenos Aires (IEGEBA), CONICET-Universidad de Buenos Aires, Buenos Aires, Argentina

    Manuel I. Stefanini, Patricia P. Iglesias, Eduardo M. Soto & Ignacio M. Soto

  3. Departamento de Ciencias Geológicas, Facultad de Ciencias Exactas y Naturales, Instituto de Estudios Andinos ‘Don Pablo Groeber’ (IDEAN, CONICET-UBA), Universidad de Buenos Aires, Buenos Aires, Argentina

    Pablo Milla Carmona

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  1. Manuel I. Stefanini
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Correspondence to Ignacio M. Soto.

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11692_2018_9444_MOESM1_ESM.xls

Plots of phenotypic (PST) differentiation compared to putative neutral genetic differentiation (FST) among populations for the male genital size (a) and first five shape variables (b–f). FST showed are those obtained from COI sequence (FSTCOI). Lines represent theoretical PST = FST as expected by neutral evolution (XLS 49 KB)

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Stefanini, M.I., Milla Carmona, P., Iglesias, P.P. et al. Differential Rates of Male Genital Evolution in Sibling Species of Drosophila. Evol Biol 45, 211–222 (2018). https://doi.org/10.1007/s11692-018-9444-0

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