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Evolutionary Consequences of Desiccation Resistance in the Male Ejaculate

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Abstract

Avoiding water loss for insects is critical for survival. Selection for reduced water loss will depend on trade-offs between resources allocated for reproduction and those allocated for resisting desiccation. However, we lack knowledge on how selection for desiccation resistance can affect the male ejaculate. Furthermore, as male ejaculate composition is complex, desiccation resistant females could evolve traits that enable them to derive longevity benefits from mating. Here, we assessed how selection for desiccation resistance impacts male testes and accessory gland size, protein content of these organs, female sperm storage and male ability to inhibit female remating behavior, in the Mexican fruit fly Anastrepha ludens. Additionally, we tested if mating increased longevity and fecundity in desiccation resistant females. Males selected for resistance to desiccation stress had smaller accessory glands and seminal vesicles and females mating with these males stored less sperm compared to control males. Females mating with resistant males had lower fecundity compared to females mating with control males. Desiccation resistant females lived longer than control females, yet this was irrespective of mating. Rapid evolutionary responses to hydric stress can have correlated effects in reproductive capabilities, which are not restricted to pre-copulatory traits. Trade-offs between resistance to desiccation stress are reflected in decreased allocation of resources to reproductive organs. Thus, production of the ejaculate may be costly for A. ludens males. Knowledge on the evolution of ejaculate traits and reproductive organ size in response to directional selection for desiccation resistance, will aid our understanding of differential sex-specific responses to environmental stress.

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References

  • Abraham, S., Lara-Pérez, L. A., Rodríguez, C., Contreras-Navarro, Y., Nuñez-Beverido, N., Ovruski, S. & Pérez-Staples, D. (2016). The male ejaculate as inhibitor of female remating in two tephritid flies. Journal of Insect Physiology, 88, 40–47.

    Article  CAS  PubMed  Google Scholar 

  • Abraham, S., Nuñez-Beverido, N., Contreras-Navarro, Y., & Pérez-Staples, D. (2014). Female receptivity in Anastrepha ludens (Diptera: Tephritidae) is not modulated by male accessory gland products. Journal of Insect Physiology, 70, 41–48.

    Article  CAS  PubMed  Google Scholar 

  • Avila, F. W., Sirot, L. K., LaFlamme, B. A., Rubinstein, C. D., & Wolfner, M. F. (2011). Insect seminal fluid proteins: Identification and function. Annual Review of Entomology, 56, 21–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradford, M. (1976). A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254.

    Article  CAS  PubMed  Google Scholar 

  • Brunel, O., & Rull, J. (2010). The natural history and unusual mating behavior of Euxesta bilimeki (Diptera: Ulidiidae). Annals of the Entomological Society of America, 103(1), 111–119.

    Article  Google Scholar 

  • Burke, M. K., & Rose, M. R. (2009). Experimental evolution with Drosophila. American Journal of Physiology—Regulatory, Integrative and Comparative Physiology, 296(6), R1847-R1854.

    Article  Google Scholar 

  • Celedonio-Hurtado, H., Aluja, M., & Liedo, P. (1995). Adult population fluctuations of Anastrepha species (Diptera: Tephritidae) in tropical orchard habitats of Chiapas, Mexico. Environmental Entomology, 24(4), 861–869.

    Article  Google Scholar 

  • Chapman, T., Herndon, L. A., Heifetz, Y., Partridge, L., & Wolfner, M. F. (2001). The Acp26Aa seminal fluid protein is a modulator of early egg hatchability in Drosophila melanogaster. Proceedings of the Royal Society of London. Series B: Biological Sciences, 268(1477), 1647.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chown, S. L., Sørensen, J. G., & Terblanche, J. S. (2011). Water loss in insects: An environmental change perspective. Journal of Insect Physiology, 57(8), 1070–1084.

    Article  CAS  PubMed  Google Scholar 

  • Cloudsley-Thompson, J. L. (1975). Adaptations of arthropoda to arid environments. Annual Review of Entomology, 20(1), 261–283.

    Article  CAS  PubMed  Google Scholar 

  • Dewsbury, D. A. (1982). Ejaculate cost and male choice. American Naturalist, 119, 601–610.

    Article  Google Scholar 

  • Edvardsson, M., & Canal, D. (2006). The effects of copulation duration in the bruchid beetle Callosobruchus maculatus. Behavioral Ecology, 17(3), 430–434.

    Article  Google Scholar 

  • Flatt, T. (2011). Survival costs of reproduction in Drosophila. Experimental Gerontology, 46(5), 369–375.

    Article  PubMed  Google Scholar 

  • Gefen, E., & Brendzel, O. (2011). Desiccation resistance and mating behaviour in laboratory populations of Drosophila simulans originating from the opposing slopes of Lower Nahal Oren (Israel). Journal of Evolutionary Biology, 24(10), 2110–2117.

    Article  CAS  PubMed  Google Scholar 

  • Gefen, E., & Gibbs, A. G. (2009). Interactions between environmental stress and male mating success may enhance evolutionary divergence of stress-resistant Drosophila populations. Evolution, 63(6), 1653–1659.

    Article  PubMed  Google Scholar 

  • Gillott, C. (2003). Male accessory gland secretions: Modulators of female reproductive physiology and behavior. Annual Review of Entomology, 48, 163–184.

    Article  CAS  PubMed  Google Scholar 

  • Goenaga, J., Mensch, J., Fanara, J. J., & Hasson, E. (2012). The effect of mating on starvation resistance in natural populations of Drosophila melanogaster. Evolutionary Ecology, 26(4), 813–823.

    Article  Google Scholar 

  • Haerty, W., Jagadeeshan, S., Kulathinal, R. J., Wong, A., Ravi Ram, K., Sirot, L. K., Levesque, L., Artieri, C. G., Wolfner, M. F., Civetta, A., et al. (2007). Evolution in the fast lane: Rapidly evolving sex-related genes in Drosophila. Genetics, 177(3), 1321–1335.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harano, T. (2012). Water availability affects female remating in the seed beetle, Callosobruchus chinensis. Ethology, 118(10), 925–931.

    Article  Google Scholar 

  • Harwood, J. F., Chen, K., Liedo, P., Muller, H. G., Wang, J. L., Morice, A. E., & Carey, J. R. (2015). Female access and diet affect insemination success, senescence, and the cost of reproduction in male Mexican fruit flies Anastrepha ludens. Physiological Entomology, 40(1), 65–71.

    Article  PubMed  PubMed Central  Google Scholar 

  • Heifetz, Y., Tram, U., & Wolfner, M. F. (2001) Male contributions to egg production: The role of accessory gland products and sperm in Drosophila melanogaster. Proceedings of the Royal Society of London. Series B: Biological Sciences, 268(1463),175.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoffmann, A. A., & Harshman, L. G. (1999) Desiccation and starvation resistance in Drosophila: Patterns of variation at the species, population and intrapopulation levels. Heredity (Edinb), 83(Pt 6), 637–643.

    Article  Google Scholar 

  • Huestis, D. L., & Lehmann, T. (2014). Ecophysiology of Anopheles gambiae s.l.: Persistence in the Sahel. Infection, Genetics and Evolution, 28, 648–661.

    Article  PubMed  PubMed Central  Google Scholar 

  • Karla, B., & Parkash, R. (2014). Trade-off of ovarian lipids and total body lipids for fecundity and starvation resistance in tropical populations of Drosophila melanogaster. Journal of Evolutionary Biology, 27(11), 2371–2385.

    Article  Google Scholar 

  • Knowles, L. L., Brodie Hernández, B., & Markow, T. A. (2005). Nonantagonistic interactions between the sexes revealed by the ecological consequences of reproductive traits. Journal of Evolutionary Biology, 18, 156–161.

    Article  Google Scholar 

  • Knowles, L. L., Hernandez, B. B., & Markow, T. A. (2004). Exploring the consequences of postmating-prezygotic interactions between the sexes. Proceedings of the Royal Society of London. Series B: Biological Sciences, 271(Suppl 5), S357–S359.

  • Kwan, L., Bedhomme, S., Prasad, N. G., & Chippindale, A. K. (2008). Sexual conflict and environmental change: Trade-offs within and between the sexes during the evolution of desiccation resistance. Journal of Genetics, 87(4), 383–394.

    Article  PubMed  Google Scholar 

  • Kwan, L., & Rundle, H. D. (2010). Adaptation to desiccation fails to generate pre- and postmating isolation in replicate Drosophila melanogaster laboratory population. Evolution, 64(3), 710–723.

    Article  PubMed  Google Scholar 

  • Liao, H. J., Qian, Q., & Liu, X. D. (2014). Heat shock suppresses mating and sperm transfer in the rice leaf folder Cnaphalocrocis medinalis. Bulletin of Entomological Research, 104(3), 383–392.

    Article  CAS  PubMed  Google Scholar 

  • Martínez, I., & Hernández-Ortiz, V. (1997) Anatomy of the reproductive system in six Anastrepha species and comments regarding their terminology in Tephritidae (Diptera). Proceedings of the Entomological Society of Washington, 99, 727–743.

    Google Scholar 

  • Matzkin, L. M., Watts, T. D., & Markow, T. A. (2009). Evolution of stress resistance in Drosophila: Interspecific variation in tolerance to desiccation and starvation. Functional Ecology, 23(3), 521–527.

    Article  Google Scholar 

  • Meza, J. S., Arredondo, J., Orozco, D., & Pérez-Staples, D. (2014). Disparity in sexual behaviour between wild and mass-reared Mexican fruit flies. Physiological Entomology, 39(3), 263–270.

    Article  Google Scholar 

  • Olsson, M., Madsen, T., & Shine, R. (1997) Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus. Proceedings of the Royal Society of London. Series B: Biological Sciences, 264, 455–459.

    Article  PubMed Central  Google Scholar 

  • Perry, J. C., Sirot, L., & Wigby, S. (2013). The seminal symphony: How to compose an ejaculate. Trends in Ecology & Evolution, 28(7), 414–422.

    Article  Google Scholar 

  • Pitnick, S., Markow, T., & Spicer, G. S. (1999). Evolution of multiple kinds of female sperm-storage organs in Drosophila. Evolution, 53(6), 1804–1822.

    Article  PubMed  Google Scholar 

  • Pitnick, S., Spicer, G. S., & Markow, T. (1997). Phylogenetic examination of female incorporation of ejaculate in Drosophila. Evolution, 51(3), 833–845.

    Article  PubMed  Google Scholar 

  • Price, P. W. (1997). Insect ecology (3rd edn.). New York: Wiley.

    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/.

  • Reinhardt, K., Dobler, R., & Abbott, J. (2016). An ecology of sperm: Sperm diversification by natural selection. Annual Review of Ecology, Evolution and Systematics, 46, 435–459.

    Article  Google Scholar 

  • Reyes-Hernández, M., & Pérez-Staples, D. (2017). Mating senescence and male reproductive organ size in the Mexican fruit fly. Physiological Entomology, 42(1), 26–35.

    Article  Google Scholar 

  • Rion, S., & Kawecki, T. J. (2007). Evolutionary biology of starvation resistance: What we have learned from Drosophila. Journal of Evolutionary Biology, 20(5), 1655–1664.

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Enriquez, C., Tadeo, E., & Rull, J. (2013). Elucidating the function of ejaculate expulsion and consumption after copulation by female Euxesta bilimeki. Behavioral Ecology and Sociobiology, 67(6), 937–946.

    Article  Google Scholar 

  • Rohmer, C., David, J. R., Moreteau, B., & Joly, D. (2004). Heat induced male sterility in Drosophila melanogaster: Adaptive genetic variations among geographic populations and role of the Y chromosome. Journal of Experimental Biology, 207, 2735–2743.

    Article  PubMed  Google Scholar 

  • Rose, M. R. (1984). Laboratory evolution of postponed senescence in Drosophila melanogaster. Evolution, 38, 1004–1010.

    Article  PubMed  Google Scholar 

  • Ruiz-Arce, R., Owen, C. L., Thomas, D. B., Barr, N. B., & McPheron, B. A. (2015). Phylogeographic structure in Anastrepha ludens (Diptera: Tephritidae) populations inferred with mtDNA sequencing. Journal of Economic Entomology, 108(3), 1324–1336.

    Article  PubMed  Google Scholar 

  • Rush, B., Sandver, S., Bruer, J., Roche, R., Wells, M., & Giebultowicz, J. (2007). Mating increases starvation resistance and decreases oxidative stress resistance in Drosophila melanogaster females. Aging Cell, 6(5), 723–726.

    Article  CAS  PubMed  Google Scholar 

  • SAS, Institute Inc. (2010). JMP ver. 7, ver. 9. SAS, Institute Inc: Carey, NC.

    Google Scholar 

  • Sassi, P. L., & Hasson, E. (2013). Desiccation resistance along an aridity gradient in the cactophilic fly Drosophila buzzatii: Sex-specific responses to stress. Evolutionary Ecology, 27(3), 505–519.

    Article  Google Scholar 

  • Service, P. M., Hutchinson, E. W., MacKinley, M. D., & Rose, M. R. (1985). Resistance to environmental stress in Drosophila melanogaster selected for postponed senescence. Physiological Zoology, 58(4), 380–389.

    Article  Google Scholar 

  • Singh, K., Samant, M. A., Tom, M. T., & Prasad, N. G. (2016) Evolution of pre- and post-copulatory traits in male Drosophila melanogaster as a correlated response to selection for resistance to cold stress. PLoS ONE, 11(4), e0153629.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sirot, L. K., Wolfner, M. F., & Wigby, S. (2011). Protein-specific manipulation of ejaculate composition in response to female mating status in Drosophila melanogaster. Proccedings of the National Academy of Science USA, 108(25), 9922–9926.

    Article  CAS  Google Scholar 

  • Stinziano, J. R., Sové, R. J., Rundle, H. D., & Sinclair, B. J. (2015). Rapid desiccation hardening changes the cuticular hydrocarbon profile of Drosophila melanogaster. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 180, 38–42.

    Article  CAS  Google Scholar 

  • Stone, A. (1942). The fruit flies of the genus Anastrepha (Miscellaneous Publication No. 439) (p. 112). Washington, DC: USDA.

    Google Scholar 

  • Taylor, P. W., Kaspi, R., & Yuval, B. (2000). Copula duration and sperm storage in Mediterranean fruit flies from a wild population. Physiological Entomology, 25, 94–99.

    Article  Google Scholar 

  • Tejeda, M. T., Arredondo, J., Liedo, P., Pérez-Staples, D., Ramos-Morales, P., & Díaz-Fleischer, F. (2016). Reasons for success: Rapid evolution for desiccation resistance and life-history changes in the polyphagous fly Anastrepha ludens. Evolution, 70(11), 2583–2594.

    Article  PubMed  Google Scholar 

  • Tejeda, M. T., Arredondo, J., Pérez-Staples, D., Ramos-Morales, P., Liedo, P., & Díaz-Fleischer, F. (2014). Effects of size, sex and teneral resources on the resistance to hydric stress in the tephritid fruit fly Anastrepha ludens. Journal of Insect Physiology, 70, 73–80.

    Article  CAS  PubMed  Google Scholar 

  • Thomas, D. B. (2003). Reproductive phenology of the Mexican fruit fly, Anastrepha ludens (Loew) (Diptera: Tephritidae) in the Sierra Madre Oriental, Northern Mexico. Neotropical Entomology, 32, 385–397.

    Article  Google Scholar 

  • Ursprung, C., den Hollander, M., & Darryl, T. G. (2009). Female seed beetles, Callosobruchus maculatus, remate for male-supplied water rather than ejaculate nutrition. Behavioral Ecology and Sociobiology, 63(6), 781–788.

    Article  Google Scholar 

  • Wedell, N., Gage, M. J. G., & Parker, G. A. (2002). Sperm competition, male prudence and sperm-limited females. Trends in Ecology and Evolution, 17, 313–320.

    Article  Google Scholar 

  • Weldon, C. W., Boardman, L., Marlin, D., & Terblanche, J. S. (2016). Physiological mechanisms of dehydration tolerance contribute to the invasion potential of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) relative to its less widely distributed congeners. Frontiers in Zoology, 13(1), 1–15.

    Article  Google Scholar 

  • Weldon, C. W., Yap, S., & Taylor, P. W. (2013). Desiccation resistance of wild and mass-reared Bactrocera tryoni (Diptera: Tephritidae). Bulletin of Entomological Research, 103(6), 690–699.

    Article  CAS  PubMed  Google Scholar 

  • Wigby, S., Perry, J. C., Kim, Y.-H., & Sirot, L. K. (2016). Developmental environment mediates male seminal protein investment in Drosophila melanogaster. Functional Ecology, 30(3), 410–419.

    Article  PubMed  Google Scholar 

  • Xu, J., & Wang, Q. (2011). Seminal fluid reduces female longevity and stimulates egg production and sperm trigger oviposition in a moth. Journal of Insect Physiology, 57(3), 385–390.

    Article  CAS  PubMed  Google Scholar 

  • Zera, A. J., & Harshman, L. G. (2001). The physiology of life history trade-offs in animals. Annual Review of Ecology and Systematics, 32(1), 95–126.

    Article  Google Scholar 

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Acknowledgements

We thank Nicolás Núñez-Beverido, Yair de Jesús Contreras, Evaristo Calihua, Carlos Carmona, Cruz Perea Castellanos, Javier Coutiño Ibarias and Desarrollo de Métodos, Programa Moscafrut (SAGARPA-SENASICA) for help throughout experiments. Enrique Alarcón and Antonio Andrade (INBIOTECA) provided access to equipment. We thank Dinesh Rao for comments to the manuscript. DPS thanks Kavita Isvaran for hosting her at the Indian Institute of Science, Bangalore, India during her sabbatical. SA was supported by a postdoctoral grant from CONICET, Argentina, MHC by a CONACyT postdoctoral scholarship, and MRH by a CONACyT doctoral scholarship. Funding was provided by the Consejo Nacional de Ciencia y Tecnología (CONACyT) Ciencia Básica Grant Number CB-2011-169887 awarded to FDF.

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Authors and Affiliations

  1. INBIOTECA, Universidad Veracruzana, Av. de las Culturas Veracruzanas 101, Col. E. Zapata, CP 91090, Xalapa, Veracruz, Mexico

    Diana Pérez-Staples, Martha Reyes-Hernández & Francisco Diaz-Fleischer

  2. Laboratorio de Investigaciones Ecoetológicas de Moscas de la Fruta y sus Enemigos Naturales (LIEMEN), PROIMI, Tucumán, Argentina

    Solana Abraham

  3. CONICET, Buenos Aires, Argentina

    Solana Abraham

  4. CONACYT– Facultad de Medicina y Cirugía, Universidad Autónoma “Benito Juárez” de Oaxaca, Ex-Hda de Aguilera S/N, C.P. 68020, Oaxaca, Oaxaca, Mexico

    Mariana Herrera-Cruz

  5. Programa Moscamed acuerdo SAGARPA-IICA, Av. Central Sur S/N, CP 30860, Metapa de Domínguez, Chiapas, Mexico

    Marco T. Tejeda

  6. Programa Moscafrut SAGARPA-SENASICA, Camino a los Cacaotales S/N, CP 30860, Metapa de Domínguez, Chiapas, Mexico

    José Arredondo

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  1. Diana Pérez-Staples
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  2. Solana Abraham
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  3. Mariana Herrera-Cruz
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  4. Martha Reyes-Hernández
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  5. Marco T. Tejeda
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  6. José Arredondo
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  7. Francisco Diaz-Fleischer
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Correspondence to Diana Pérez-Staples.

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Pérez-Staples, D., Abraham, S., Herrera-Cruz, M. et al. Evolutionary Consequences of Desiccation Resistance in the Male Ejaculate. Evol Biol 45, 56–66 (2018). https://doi.org/10.1007/s11692-017-9429-4

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