Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

The rapid diversification of sexual traits is a common phenomenon accompanying the evolution of reproductive isolation, yet the evolutionary mechanisms driving such diversification are often unknown. Based on experimentally evolved strains of two sister species of cactophilic Drosophila, we investigated the correlated evolution of primary and secondary sexual traits to semi-natural environments enriched in secondary metabolites. We compared patterns of morphological evolution in the size and shape of male wing and genitalia of Drosophila buzzatii and Drosophila koepferae selected for different levels of alkaloid intensities for 20 generations. We found similar modes of selection operating among organs but not among species. The evolution of these traits in D. koepferae were compatible with patterns of stabilizing selection, while in D. buzzatii were characterized by directional changes. We also found that allometric variation was an important component of genital shape evolution, whereas changes in the wing morphology were less pronounced and mostly non-allometric. Overall, our data suggest that the diversification of sexual traits in this species pair is related to the evolution of dissimilar genetic architectures and reinforced by divergent ecological responses. © 2018, Springer Nature Switzerland AG.

Registro:

Documento: Artículo
Título:Divergent patterns of correlated evolution in primary and secondary sexual traits of cactophilic Drosophila
Autor:Padró, J.; Vrdoljak, J.; Milla Carmona, P.; Soto, I.M.
Filiación:Instituto de Ecología, Genética y Evolución de Buenos Aires (IEGEBA – CONICET), DEGE, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Int. Guiraldes, Buenos Aires, 2160, Argentina
Ecotono Laboratory, INIBIOMA, CONICET, Universidad Nacional del Comahue, Quintral 1250, Bariloche, 8400, Argentina
Instituto Patagónico para el Estudio de los Ecosistemas Continentales, Consejo Nacional de Investigaciones Científicas y Técnicas (IPEEC-CONICET), Boulevard Almirante Brown 2915, Puerto Madryn, Chubut U9120ACD, Argentina
Laboratorio de Ecosistemas Marinos Fósiles, Instituto de Estudios Andinos Don Pablo Groeber (CONICET-UBA), Intendente Güiraldes 2160, Ciudad Universitaria, Buenos Aires, C1428EHA, Argentina
Palabras clave:Alkaloid; Chemical stress; Experimental evolution; Genitalia; Morphological evolution; Wing; Drosophila buzzatii; Drosophila koepferae
Año:2019
Volumen:33
Número:1
Página de inicio:71
Página de fin:87
DOI: http://dx.doi.org/10.1007/s10682-018-9964-1
Título revista:Evolutionary Ecology
Título revista abreviado:Evol. Ecol.
ISSN:02697653
CODEN:EVECE
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_02697653_v33_n1_p71_Padro

Referencias:

  • Arnqvist, G., The evolution of animal genitalia: distinguishing between hypotheses by single species studies (1997) Biol J Linn Soc, 60, pp. 365-379
  • Arnqvist, G., Thornhill, R., Evolution of animal genitalia: patterns of phenotypic and genotypic variation and condition dependence of genital and non-genital morphology in water strider (Heteroptera: Gerridae: Insecta) (1998) Genet Res, 71 (3), pp. 193-212
  • Badyaev, A.V., Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation (2005) Proc R Soc Lond B Biol Sci, 272 (1566), pp. 877-886
  • Barker, J.S.F., Starmer, W.T., (1982) Ecological genetics and evolution: the cactus-yeast-Drosophila model system, , (eds), Academic Press, Cambridge
  • Blows, M.W., Brooks, R., Kraft, P.G., Exploring complex fitness surfaces: multiple ornamentation and polymorphism in male guppies (2003) Evolution, 57 (7), pp. 1622-1630
  • Bonhomme, V., Picq, S., Gaucherel, C., Claude, J., Momocs: outline analysis using R (2014) J Stat Softw, 56, pp. 1-24
  • Brazner, J.C., Etges, W.J., Pre-mating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. II. Effects of larval substrates on time to copulation, mate choice and mating propensity (1993) Evol Ecol, 7 (6), pp. 605-624
  • Brodie, E.D., Moore, A.J., Janzen, F.J., Visualizing and quantifying natural selection (1995) Trends Ecol Evol, 10 (8), pp. 313-318
  • Carreira, V.P., Soto, I.M., Mensch, J., Fanara, J.J., Genetic basis of wing morphogenesis in Drosophila: sexual dimorphism and non-allometric effects of shape variation (2011) BMC Dev Biol, 11 (1), p. 32
  • Chippindale, A.K., Chu, T.J., Rose, M.R., Complex trade-offs and the evolution of starvation resistance in Drosophila melanogaster (1996) Evolution, 50 (2), pp. 753-766
  • Chippindale, A.K., Gibbs, A.G., Sheik, M., Yee, K.J., Djawdan, M., Bradley, T.J., Rose, M.R., Resource acquisition and the evolution of stress resistance in Drosophila melanogaster (1998) Evolution, 52 (5), pp. 1342-1352
  • Colines, B., Soto, I.M., de Panis, D.N., Padró, J., Experimental hybridization in allopatric species of the Drosophila repleta group (Diptera: Drosophilidae): implications for the mode of speciation (2018) Biol J Linn Soc, 123 (2), pp. 290-301
  • Coyne, J.A., The genetics of an isolating mechanism between two sibling species of Drosophila (1993) Evolution, 47, pp. 778-788
  • De Panis, D.N., Padró, J., Furió-Tarí, P., Tarazona, S., Milla Carmona, P.S., Soto, I.M., Dopazo, H., Hasson, E., Transcriptome modulation during host shift is driven by secondary metabolites in desert Drosophila (2016) Mol Ecol, 25 (18), pp. 4534-4550
  • Debat, V., Bégin, M., Legout, H., David, J.R., Allometric and nonallometric components of Drosophila wing shape respond differently to developmental temperature (2003) Evolution, 57 (12), pp. 2773-2784
  • Dryden, I.L., Mardia, K.V., (1998) Statistical shape analysis, , Wiley, London
  • Ehrlich, P.R., Raven, P.H., Butterflies and plants: a study in coevolution (1964) Evolution, 18 (4), pp. 586-608
  • Etges, W.J., Premating isolation is determined by larval substrates in cactophilic Drosophila mojavensis (1992) Evolution, 46, pp. 1945-1950
  • Etges, W.J., Tripodi, A.D., Premating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. VIII. Mating success mediated by epicuticular hydrocarbons within and between isolated populations (2008) J Evol Biol, 21 (6), pp. 1641-1652
  • Fanara, J.J., Soto, I.M., Lipko, P., Hasson, E., First record of Drosophila buzzatii (Patterson & Wheeler)(Diptera: Drosophilidae) emerging from a non-cactus host (2016) Neotrop Entomol, 45 (3), pp. 333-335
  • Franco, F.F., Manfrin, M.H., Recent demographic history of cactophilic Drosophila species can be related to quaternary palaeoclimatic changes in South America (2013) J Biogeogr, 40 (1), pp. 142-154
  • Gidaszewski, N.A., Baylac, M., Klingenberg, C.P., Evolution of sexual dimorphism of wing shape in the Drosophila melanogaster subgroup (2009) BMC Evol Biol, 9 (1), p. 110
  • Gilchrist, A.S., Partridge, L., A comparison of the genetic basis of wing size divergence in three parallel body size clines of Drosophila melanogaster (1999) Genetics, 153 (4), pp. 1775-1787
  • Gilchrist, A.S., Partridge, L., The contrasting genetic architecture of wing size and shape in Drosophila melanogaster (2001) Heredity, 86 (2), pp. 144-152
  • Harshman, L.G., Hoffmann, A.A., Clark, A.G., Selection for starvation resistance in Drosophila melanogaster: physiological correlates, enzyme activities and multiple stress responses (1999) J Evol Biol, 12 (2), pp. 370-379
  • Heinen-Kay, J.L., Noel, H.G., Layman, C.A., Langerhans, R.B., Human-caused habitat fragmentation can drive rapid divergence of male genitalia (2014) Evol Appl, 7 (10), pp. 1252-1267
  • Hoffmann, A.A., Hercus, M.J., Environmental stress as an evolutionary force (2000) Bioscience, 50 (3), pp. 217-226
  • Hoikkala, A., Aspi, J., Criteria of female mate choice in Drosophila littoralis, D. montana, and D. ezoana (1993) Evolution, 47 (3), pp. 768-777
  • House, C.M., Lewis, Z., Hodgson, D.J., Wedell, N., Sharma, M.D., Hunt, J., Hosken, D.J., Sexual and natural selection both influence male genital evolution (2013) PLoS ONE, 8 (5)
  • Hurtado, J., Soto, E.M., Orellana, L., Hasson, E., Mating success depends on rearing substrate in cactophilic Drosophila (2012) Evol Ecol, 26, pp. 733-743
  • Hurtado, J., Iglesias, P.P., Lipko, P., Hasson, E., Multiple paternity and sperm competition in the sibling species Drosophila buzzatii and Drosophila koepferae (2013) Mol Ecol, 22 (19), pp. 5016-5026
  • Iglesias, P.P., Soto, E.M., Soto, I.M., Colines, B., Hasson, E., The influence of developmental environment on courtship song in cactophilic Drosophila (2018) J Evol Biol
  • Iwata, H., Ukai, Y., SHAPE: a computer program package for quantitative evaluation of biological shapes based on elliptic fourier descriptors (2002) J Hered, 93, pp. 384-385
  • Jagadeeshan, S., Singh, R.S., A time-sequence functional analysis of mating behaviour and genital coupling in Drosophila: role of cryptic female choice and male sex-drive in the evolution of male genitalia (2006) J Evol Biol, 19, pp. 1058-1070
  • Klingenberg, C.P., MorphoJ: an integrated software package for geometric morphometrics (2011) Mol Ecol Res, 11 (2), pp. 353-357
  • Klingenberg, C.P., Marugán-Lobón, J., Evolutionary covariation in geometric morphometric data: analyzing integration, modularity, and allometry in a phylogenetic context (2013) Syst Biol, 62 (4), pp. 591-610
  • Krebs, R.A., Barker, J.S.F., Coexistence of ecologically similar colonising species. II. Population differentiation in Drosophila aldrichi and D. buzzatii for competitive effects and responses at different temperatures and allozyme variation in D. aldrichi (1993) J Evol Biol, 6 (2), pp. 281-298
  • Kuhl, F.P., Giardina, C.R., Elliptic Fourier features of a closed contour (1982) Comput Gr Image Process, 18, pp. 236-258
  • Langerhans, R.B., Anderson, C.M., Heinen-Kay, J.L., Causes and consequences of genital evolution (2016) Integr Comp Biol, 56 (4), pp. 741-751
  • Lorch, P.D., Proulx, S., Rowe, L., Day, T., Condition-dependent sexual selection can accelerate adaptation (2003) Evol Ecol Res, 5 (6), pp. 867-881
  • Manfrin, M.H., Sene, F.M., Cactophilic Drosophila in South America: a model for evolutionary studies (2006) Genetica, 126, pp. 57-75
  • Manfrin, M.H., De Brito, R.O.A., Sene, F.M., Systematics and evolution of the Drosophila buzzatii (Diptera: Drosophilidae) cluster using mtDNA (2001) Ann Entomol Soc Am, 94 (3), pp. 333-346
  • Mardia, K.V., Bookstein, F.L., Moreton, I.J., Statistical assessment of bilateral symmetry of shapes (2000) Biometrika, 2, pp. 285-300
  • Markow, T.A., O’Grady, P.M., Evolutionary genetics of reproductive behavior in Drosophila: connecting the dots (2005) Annu Rev Genet, 39, pp. 263-291
  • Menezes, B.F., Vigoder, F.M., Peixoto, A.A., Varaldi, J., Bitner-Mathé, B.C., The influence of male wing shape on mating success in Drosophila melanogaster (2013) Anim Behav, 85 (6), pp. 1217-1223
  • Meyer, J.M., Fogleman, J.C., Significance of saguaro cactus alkaloids in ecology of Drosophila mettleri, a soil-breeding, cactophilic drosophilid (1987) J Chem Ecol, 13 (11), pp. 2069-2081
  • Ogunbodede, O., McCombs, D., Trout, K., Daley, P., Terry, M., New mescaline concentrations from 14 taxa/cultivars of Echinopsis spp. (Cactaceae) (“San Pedro”) and their relevance to shamanic practice (2010) J Ethnopharmacol, 131 (2), pp. 356-362
  • Padró, J., Carreira, V., Corio, C., Hasson, E., Soto, I.M., Host alkaloids differentially affect developmental stability and wing vein canalization in cactophilic Drosophila buzzatii (2014) J Evol Biol, 27 (12), pp. 2781-2797
  • Padró, J., De Panis, D.N., Vrdoljak, J., Carmona, P.M., Colines, B., Hasson, E., Soto, I.M., Experimental evolution of alkaloid tolerance in sibling Drosophila species with different degrees of specialization (2018) Evol Biol, 45 (2), pp. 170-181
  • Panhuis, T.M., Butlin, R., Zuk, M., Tregenza, T., Sexual selection and speciation (2001) Trends Ecol Evol, 16, pp. 364-371
  • Parsons, P.A., Morphological stasis: an energetic and ecological perspective incorporating stress (1994) J Theor Biol, 171 (4), pp. 409-414
  • Partridge, L., Ewing, A., Chandler, A., Male size and mating success in Drosophila melanogaster: the roles of male and female behaviour (1987) Anim Behav, 35 (2), pp. 555-562
  • Piccinali, R., Aguadé, M., Hasson, E., Comparative molecular population genetics of the Xdh locus in the cactophilic sibling species Drosophila buzzatii and D. koepferae (2004) Mol Biol Evol, 21 (1), pp. 141-152
  • (2017) R: a language and environment for statistical computing, , R Foundation for Statistical Computing, Vienna
  • Reinhardt, K., Natural selection and genital variation: a role for the environment, parasites and sperm ageing? (2010) Genetica, 138 (1), pp. 119-127
  • Reti, L., Castrillón, J.A., Cactus alkaloids. I. Trichocereus terscheckii (Parmentier) Britton and Rose (1951) J Am Chem Soc, 73, pp. 1767-1769
  • Richmond, M.P., The role of aedeagus size and shape in failed mating interactions among recently diverged taxa in the Drosophila mojavensis species cluster (2014) BMC Evol Biol, 14 (1), p. 255
  • Richmond, M.P., Johnson, S., Markow, T.A., Evolution of reproductive morphology among recently diverged taxa in the Drosophila mojavensis species cluster (2012) Ecol Evol, 2 (2), pp. 397-408
  • Roff, D.A., Trade-offs between growth and reproduction: an analysis of the quantitative genetic evidence (2000) J Evol Biol, 13 (3), pp. 434-445
  • Rohlf, F.J., The tps series of software (2015) Hystrix, 26 (1), pp. 9-12
  • Rosenthal, G.A., Berenbaum, M.R., (2012) Herbivores: their interactions with secondary plant metabolites: ecological and evolutionary processes, 2. , Academic Press, London
  • Santos, M., Ruiz, A., Barbadilla, A., Quezada-Díaz, J.E., Hasson, E., Fontdevila, A., The evolutionary history of Drosophila buzzatii. XlV. Larger flies mate more often in nature (1988) Heredity, 61, pp. 255-262
  • Sgro, C.M., Hoffmann, A.A., Genetic correlations, tradeoffs and environmental variation (2004) Heredity, 93 (3), p. 241
  • Simmons, L.W., House, C.M., Hunt, J., García-González, F., Evolutionary response to sexual selection in male genital morphology (2009) Curr Biol, 19 (17), pp. 1442-1446
  • Soto, I.M., Aedeagal divergence in sympatric populations of two sibling species of cactophilic Drosophila (Diptera: Drosophilidae): evidence of character displacement? (2012) Neotrop Entomol, 41 (3), pp. 207-213
  • Soto, I.M., Carreira, V.P., Fanara, J.J., Hasson, E., Evolution of male genitalia: environmental and genetic factors affect genital morphology in two Drosophila sibling species and their hybrids (2007) BMC Evol Biol, 7, p. 1
  • Soto, I.M., Carreira, V.P., Soto, E.M., Hasson, E., Wing morphology and fluctuating asymmetry depend on the host plant in cactophilic Drosophila (2008) J Evol Biol, 21 (2), pp. 598-609
  • Soto, I.M., Carreira, V.P., Soto, E.M., Márquez, F., Lipko, P., Hasson, E., Rapid divergent evolution of male genitalia among populations of Drosophila buzzatii (2013) Evol Biol, 40, pp. 395-407
  • Soto, I.M., Carreira, V.P., Corio, C., Padró, J., Soto, E.M., Hasson, E., Differences in tolerance to host cactus alkaloids in Drosophila koepferae and D. buzzatii (2014) PLoS ONE, 9 (2)
  • (2001) Statistica User’s Guide, , Release 6.0 Edition, StatSoft Inc., Tulsa, OK
  • Stefanini, M.I., Carmona, P.M., Iglesias, P.P., Soto, E.M., Soto, I.M., Differential rates of male genital evolution in sibling species of Drosophila (2018) Evol Biol, 45, pp. 211-222
  • Trotta, V., Cavicchi, S., Guerra, D., Andersen, D.H., Babbitt, G.A., Kristensen, T.N., Pedersen, K.S., Pertoldi, C., Allometric and non-allometric consequences of inbreeding on Drosophila melanogaster wings (2011) Biol J Linn Soc, 102 (3), pp. 626-634
  • Van Doorn, G.S., Edelaar, P., Weissing, F.J., On the origin of species by natural and sexual selection (2009) Science, 326, pp. 1704-1707
  • Zahavi, A., Mate selection—a selection for a handicap (1975) J Theor Biol, 53 (1), pp. 205-214

Citas:

---------- APA ----------
Padró, J., Vrdoljak, J., Milla Carmona, P. & Soto, I.M. (2019) . Divergent patterns of correlated evolution in primary and secondary sexual traits of cactophilic Drosophila. Evolutionary Ecology, 33(1), 71-87.
http://dx.doi.org/10.1007/s10682-018-9964-1
---------- CHICAGO ----------
Padró, J., Vrdoljak, J., Milla Carmona, P., Soto, I.M. "Divergent patterns of correlated evolution in primary and secondary sexual traits of cactophilic Drosophila" . Evolutionary Ecology 33, no. 1 (2019) : 71-87.
http://dx.doi.org/10.1007/s10682-018-9964-1
---------- MLA ----------
Padró, J., Vrdoljak, J., Milla Carmona, P., Soto, I.M. "Divergent patterns of correlated evolution in primary and secondary sexual traits of cactophilic Drosophila" . Evolutionary Ecology, vol. 33, no. 1, 2019, pp. 71-87.
http://dx.doi.org/10.1007/s10682-018-9964-1
---------- VANCOUVER ----------
Padró, J., Vrdoljak, J., Milla Carmona, P., Soto, I.M. Divergent patterns of correlated evolution in primary and secondary sexual traits of cactophilic Drosophila. Evol. Ecol. 2019;33(1):71-87.
http://dx.doi.org/10.1007/s10682-018-9964-1