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Does body size influence mating success? A morphometric study of two Anastrepha (Diptera: Tephritidae) fruit fly species

Published online by Cambridge University Press:  20 September 2021

Mayren Sánchez-Rosario Open the ORCID record for Mayren Sánchez-Rosario [Opens in a new window] ,
Diana Pérez-Staples Open the ORCID record for Diana Pérez-Staples [Opens in a new window] ,
Javier Valle-Mora Open the ORCID record for Javier Valle-Mora [Opens in a new window] ,
Daniel Sánchez-Guillén ,
Lorena Ruiz-Montoya Open the ORCID record for Lorena Ruiz-Montoya [Opens in a new window]  and
Pablo Liedo Open the ORCID record for Pablo Liedo [Opens in a new window]
Mayren Sánchez-Rosario*
Affiliation:
El Colegio de la Frontera Sur (ECOSUR), Carretera Antiguo Aeropuerto, C.P. 30700, Tapachula, Chiapas, México
Diana Pérez-Staples
Affiliation:
INBIOTECA, Universidad Veracruzana, Av. de las Culturas Veracruzanas, No.101, Col. E. Zapata, C.P. 91090, Xalapa, Veracruz, México
Javier Valle-Mora
Affiliation:
El Colegio de la Frontera Sur (ECOSUR), Carretera Antiguo Aeropuerto, C.P. 30700, Tapachula, Chiapas, México
Daniel Sánchez-Guillén
Affiliation:
El Colegio de la Frontera Sur (ECOSUR), Carretera Antiguo Aeropuerto, C.P. 30700, Tapachula, Chiapas, México
Lorena Ruiz-Montoya
Affiliation:
El Colegio de la Frontera Sur (ECOSUR), Carretera Panamericana y Periférico Sur, Barrio María Auxiliadora, C.P. 29290, San Cristóbal de las Casas, Chiapas, México
Pablo Liedo
Affiliation:
El Colegio de la Frontera Sur (ECOSUR), Carretera Antiguo Aeropuerto, C.P. 30700, Tapachula, Chiapas, México
*
Author for correspondence: Mayren Sánchez Rosario, Email: [email protected]
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Abstract

Male mating success depends on various traits and factors, and correctly identifying these traits can be key in the context of pest management. For tephritid pests, controlled through the sterile insect technique (SIT) traits, such as male size, can be manipulated through mass-rearing procedures. Thus, it is particularly important to understand whether male size can favor mating success. Here, we evaluated mating success of males of different sizes in Anastrepha ludens and Anastrepha obliqua, two species controlled through SIT. For both species, a morphometric analysis was performed of mated and unmated mass-reared and wild males in field cages. In both A. ludens and A. obliqua, wild females did not discriminate their mates based on male size and mated more frequently with wild males regardless of size. For mass-reared males, we found no evidence of an advantage of the large males compared to small males in mating success. However, we did find differences between the morphometric traits of mass-reared and wild males. In A. ludens, traits associated to mating success were Face Width (FW), Head Width (HW), Thorax Length (TL) and Wing Length (WL), and for A. obliqua were FW, HW, WL and WW (Wing Width). Overall, FW and TL were more consistent predictors of mating success. In conclusion, female choice seems to suggest multivariate selection, confirming that overall body size (expressed as pupal diameter, which is highly correlated with weight) is not a decisive factor in male mating success in these two species. However, morphological traits such as FW, HW, TL, WL and WW may be relevant in mating preference of wild female.

Keywords

Anastrepha ludensAnastrepha obliquafemale choicemorphometric traitssexual behaviorsterile insect technique
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 112 , Issue 3 , June 2022 , pp. 298 - 310
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Aluja, M and Mangan, RL (2008) Fruit fly (Diptera: Tephritidae) host status determination: critical conceptual, methodological, and regulatory considerations. Annual Review of Entomology 53, 473–502.CrossRefGoogle ScholarPubMed
Aluja, M, Piñero, J, Jácome, I, Díaz-Fleischer, F and Sivinski, J (2000) Behavior of flies in the genus Anastrepha (Trypetinae: Toxotrypanini). In Aluja, M and Norrbom, AL (eds), Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. Boca Raton, FL, USA: CRC Press, pp. 375–406.Google Scholar
Aluja, M, Pérez-Staples, D, Sivinski, J, Sánchez, A and Piñero, J (2008) Effects of male condition on fitness in two tropical tephritid flies with contrasting life histories. Animal Behaviour 76, 1997–2009.10.1016/j.anbehav.2008.08.020CrossRefGoogle Scholar
Aluja, M, Rull, J, Sivinski, J, Trujillo, G and Pérez-Staples, D (2009) Male and female condition influence mating performance and sexual receptivity in two tropical fruit flies (Diptera: Tephritidae) with contrasting life histories. Journal of Insect Physiology 55, 1091–1098.CrossRefGoogle ScholarPubMed
Anjos-Duarte, CS, Costa, AM and Joachim-Bravo, IS (2011) Sexual behavior of the Mediterranean fruit fly (Diptera: Tephritidae): the influence of female size on mate choice. Journal of Applied Entomology 135, 367–373.10.1111/j.1439-0418.2010.01552.xCrossRefGoogle Scholar
Arita, LH and Kaneshiro, KY (1988) Body size and differential mating success between males of two populations of the Mediterranean fruit fly. Pacific Science 42, 173–177.Google Scholar
Bachmann, GE, Devescovi, F, Nussenbaum, AL, Milla, FH, Todd, SE, Cladera, JE, Fernández, PC, Vera, MT and Segura, DF (2019) Mate choice confers direct benefits to females of Anastrepha fraterculus (Diptera: Tephritidae). PLoS ONE 14, 1–14.10.1371/journal.pone.0214698CrossRefGoogle Scholar
Bates, D, Maechler, M, Bolker, B and Walker, S (2020) lme4: Fit linear and generalized linear mixed-effects models. R package version 1.1-23, Available at https://cran.r-project.org/web/packages/lme4/index.html.Google Scholar
Benelli, G, Donati, E, Romano, D, Ragni, G, Bonsignori, G, Stefanini, C and Canale, A (2015) Is bigger better? Male body size affects wing-borne courtship signals and mating success in the olive fruit fly, Bactrocera oleae (Diptera: Tephritidae). Insect Science 23, 869–880.CrossRefGoogle Scholar
Blanckenhorn, WU (2000) The evolution of body size: what keeps organisms small? The Quarterly Review of Biology 75, 385–407.CrossRefGoogle ScholarPubMed
Bonduriansky, R and Day, T (2003) The evolution of static allometry in sexually selected traits. Evolution 57, 2450–2458.CrossRefGoogle ScholarPubMed
Burk, T and Webb, JC (1983) Effect of male size on calling propensity, song parameters, and mating success in Caribbean fruit flies, Anastrepha suspensa (Loew) (Diptera: Tephritidae). Annals of the Entomological Society of America 76, 678–682.CrossRefGoogle Scholar
Calkins, CO and Webb, JC (1983) A cage and support framework for behavioral tests of fruit flies in the field. Florida Entomologist 66, 512–514.CrossRefGoogle Scholar
Cayol, JP (2000) Changes in sexual behavior and life history traits of tephritid species caused by mass-rearing processes. In Aluja, M and Norrbom, AL (eds), Fruit Flies (Diptera: Tephritidae): Phylogeny and Evolution of Behavior. Boca Raton, FL, USA, CRC Press, pp. 843–860.Google Scholar
Churchill-Stanland, C, Stanland, R, Wong, TTY, Tanaka, N, McInnis, DO and Dowell, RV (1986) Size as a factor in the mating propensity of the Mediterranean fruit flies, Ceratitis capitata (Diptera: Tephritidae), in the laboratory. Journal of Economic Entomology 79, 614–619.CrossRefGoogle Scholar
De Aquino, JC and Joachim-Bravo, IS (2014) Relevance of male size to female mate choice in Ceratitis capitata (Diptera: Tephritidae): investigations with wild and laboratory-reared flies. Journal of Insect Behavior 27, 162–176.CrossRefGoogle Scholar
De Souza, JM, de Lima-Filho, PA, Molina, WF, de Almeida, LM, de Gouveia, MB, de Macêdo, FP, Laumann, RA and Paranhos, BA (2015) Wing morphometry and acoustic signals in sterile and wild males: implications for mating success in Ceratitis capitata. Scientific World Journal 2015, 526969. doi: 10.1155/2015/526969CrossRefGoogle ScholarPubMed
Díaz-Fleischer, F and Aluja, M (2000) Behavior of Tephritid flies: a historical perspective. In Aluja, M and Norrbom, AL (eds), Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. Boca Raton, FL, USA: CRC Press, pp. 39–69.Google Scholar
Ekanayake, EWMTD, Jayasundara, MSH, Peek, T, Clarke, AR and Schutze, MK (2017) Effect of body size, age, and premating experience on male mating success in Bactrocera tryoni (Diptera: Tephritidae). Journal of Economic Entomology 110, 2278–2281.10.1093/jee/tox186CrossRefGoogle Scholar
Ekesi, S, De Meyer, M, Mohamed, SA, Virgilo, M and Borgemeister, C (2016) Taxonomy, ecology, and management of native and exotic fruit fly species in Africa. Annual Review of Entomology 61, 219–238.CrossRefGoogle ScholarPubMed
Enkerlin, WR (2005) Impact of fruit fly control programs using the sterile insect technique. In Dyck, A, Hendrichs, J and Robinson, AS (eds), Sterile Insect Technique: Principles and Practice in Area Wide Integrated Pest Management. Dordrecht, The Netherlands: Springer, pp. 651–676.CrossRefGoogle Scholar
FAO/IAEA/USDA (2019) Product Quality Control for Sterile Mass-reared and Released Tephritid Fruit Flies. Version 7.0. Vienna, Austria, International Atomic Energy Agency.Google Scholar
Field, SA and Yuval, B (1999) Nutritional status affects copula duration in the Mediterranean fruit fly, Ceratitis capitata (Insecta Tephritidae). Ethology Ecology & Evolution 11, 61–70.CrossRefGoogle Scholar
Fox, J and Bouchet-Valat, M (2020) Rcmdr: R Commander. R package version 2.7-0. Available at https://CRAN.R-project.org/package=Rcmdr.Google Scholar
Fox, J and Weisberg, S (2020) Car: an R Companion to Applied Regression. R package version 3.0-9. Available at https://CRAN.R-project.org/package=car.Google Scholar
Friendly, M and Fox, J (2020) Candisc: Visualizing generalized canonical discriminant and canonical correlation analysis. R package version 0.8-3. Available at https://cran.r-project.org/package=candisc.Google Scholar
Gómez-Cendra, PV, Segura, DF, Alberti, AC and Vilardi, JC (2014) Morphometric trait differentiation between a wild and a mass reared population of Anastrepha fraterculus (Diptera: Tephritidae). International Journal of Tropical Insect Science 34, S82–S89.CrossRefGoogle Scholar
Gómez-Cendra, PV, Paulin, LE, Oroño, L, Ovruski, SM and Vilardi, JC (2016) Morphometric differentiation among Anastrepha fraterculus (Diptera: Tephritidae) exploiting sympatric alternate hosts. Environmental Entomology 45, 508–517.CrossRefGoogle ScholarPubMed
Hasson, O and Rossler, Y (2002) Character-specific homeostasis dominates fluctuating asymmetries in the medfly (Diptera: Tephritidae). Florida Entomologist 85, 73–82.CrossRefGoogle Scholar
Hernández, E, Ruíz-Montoya, L, Toledo, J, Montoya, P, Liedo, P, Aceituno-Medina, M and Perales, H (2019) A comparison of sexual competitiveness and demographic traits of Anastrepha obliqua (Macquart) (Diptera: Tephritidae) among fruit-associated populations. Bulletin of Entomological Research 109, 333–341.CrossRefGoogle ScholarPubMed
Hunt, MK, Crean, CS, Wood, RJ and Gilburn, AS (1998) Fluctuating asymmetry and sexual selection in the Mediterranean fruit fly (Diptera, Tephritidae). Biological Journal of the Linnean Society 64, 385–396.10.1111/j.1095-8312.1998.tb00339.xCrossRefGoogle Scholar
Jagadeeshan, S, Shah, U, Chakrabarti, D and Singh, RS (2015) Female choice or male sex drive? The advantages of male body size during mating in Drosophila melanogaster. PLoS ONE 10, 1–12.CrossRefGoogle ScholarPubMed
Joachim-Bravo, IS, Anjos, CS and Costa, AM (2009) The role of protein in the sexual behaviour of males of Ceratitis capitata (Diptera: Tephritidae): mating success, copula duration and number of copulations. Zoologia (Curitiba) 26, 407–412.CrossRefGoogle Scholar
Kirkpatrick, M and Ryan, MJ (1991) The evolution of mating preferences and the paradox of the lek. Nature 350, 33–38.CrossRefGoogle Scholar
Knipling, EF (1955) Possibilities of insect control or eradication through the use of sexually sterile males. Journal of Economic Entomology 48, 459–462.CrossRefGoogle Scholar
Lance, DR and McInnis, DO (2005) Biological basis of the sterile insect technique. In Dyck, VA, Hendrichs, J and Robinson, AS (eds), Sterile Insect Technique: Principles and Practice in Area Wide Integrated Pest Management. Dordrecht, The Netherlands: Springer, pp. 69–94.10.1007/1-4020-4051-2_3CrossRefGoogle Scholar
Liaw, A and Wiener, M (2018) randomForest: Breiman and Cutler's Random Forests for classification and regression. R package version 4.6-14. Available at https://www.stat.berkeley.edu/~breiman/RandomForests/.Google Scholar
Liedo, P, Carey, JR, Celedonio, H and Guillen, J (1992) Size specific demography of three species of Anastrepha fruit flies. Entomologia Experimentalis et Applicata 63, 135–142.CrossRefGoogle Scholar
McInnis, DO (1987) Mediterranean Fruit fly (Diptera: Tephritidae): directional selection for large and small pupal size. Annals of the Entomological Society of America 80, 333–338.10.1093/aesa/80.3.333CrossRefGoogle Scholar
Meza-Hernández, JS and Díaz-Fleischer, F (2006) Comparison of sexual compatibility between laboratory and wild Mexican fruit flies under laboratory and field conditions. Journal of Economic Entomology 99, 1979–1986.CrossRefGoogle ScholarPubMed
Niyazi, N, Shuker, DM and Wood, RJ (2008) Male position and calling effort together influence male attractiveness in leks of the medfly, Ceratitis capitata (Diptera: Tephritidae). Biological Journal of the Linnean Society 95, 479–487.CrossRefGoogle Scholar
Norry, FM, Calcagno, G, Vera, MT, Manso, F and Vilardi, JC (1999) Sexual selection on male morphology independent of male-male competition in the Mediterranean fruit fly (Diptera: Tephritidae). Annals of the Entomological Society of America 92, 571–577.CrossRefGoogle Scholar
Orozco-Dávila, D, Quintero, JL, Hernández, E, Solís, E, Artiaga, T, Hernández, R, Ortega, C and Montoya, P (2017) Mass rearing and sterile insect releases for the control of Anastrepha spp. pests in Mexico – a review. Entomologia Experimentalis et Applicata 164, 176–187.CrossRefGoogle Scholar
Orozco, D and López, RO (1993) Mating competitiveness of wild and laboratory mass-reared medflies: effect of male size. In Aluja, M and Liedo, P (eds), Fruit Flies: Biology and Management. New York, Springer-Verlag, pp. 185–188.10.1007/978-1-4757-2278-9_34CrossRefGoogle Scholar
Pérez-Staples, D and Aluja, M (2004) Anastrepha striata (Diptera: Tephritidae) females that mate with virgin males live longer. Annals of the Entomological Society of America 97, 1336–1341.CrossRefGoogle Scholar
Pérez-Staples, D, Weldon, CW, Radhakrishnan, P, Prenter, J and Taylor, PW (2010) Control of copula duration and sperm storage by female Queensland fruit flies. Journal of Insect Physiology 56, 1755–1762.CrossRefGoogle ScholarPubMed
Pérez-Staples, D, Shelly, T and Yuval, B (2013) Female mating failure and the ‘failure’ of mating in sterile insect programs. Entomologia Experimentalis et Applicata 146, 66–78.CrossRefGoogle Scholar
R Core Team (2020) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Robacker, DC, Mangan, RL, Moreno, DS and Tarshis Moreno, AM (1991) Mating behavior and male mating success in wild Anastrepha ludens (Diptera: Tephritidae) on a field-caged host tree. Journal of Insect Behavior 4, 471–487.CrossRefGoogle Scholar
Robinson, AS, Cayol, JP and Hendrichs, J (2002) Recent findings on medfly sexual behavior: implications for SIT. Florida Entomologist 85, 171–181.CrossRefGoogle Scholar
Rodriguero, MS, Vera, MT, Rial, E, Cayol, JP and Vilardi, JC (2002 a) Sexual selection on multivariate phenotype in wild and mass-reared Ceratitis capitata (Diptera: Tephritidae). Heredity 89, 480–487.CrossRefGoogle Scholar
Rodriguero, MS, Vilardi, JC, Vera, MT, Cayol, JP and Rial, E (2002 b) Morphometric traits and sexual selection in medfly (Diptera: Tephritidae) under field cage conditions. Florida Entomologist 85, 143–149.CrossRefGoogle Scholar
Roriz, A, Japyassú, H and Joachim-Bravo, I (2018) Courtship in two morphotypes of the Anastrepha fraterculus (Diptera: Tephritidae) cryptic species complex and their implications for understanding mate recognition. Journal of Insect Behavior 31, 535–551.CrossRefGoogle Scholar
Roriz, A, Japyassú, H, Cáceres, C, Teresa, V and Joachim-Bravo, I (2019) Pheromone emission patterns and courtship sequences across distinct populations within Anastrepha fraterculus (Diptera: Terphitidae) cryptic species complex. Bulletin of Entomological Research 109, 408–417.10.1017/S0007485318000846CrossRefGoogle Scholar
Schutze, MK, Dammalage, T, Jessup, A, Vreysen, MJB, Wornoayporn, V and Clarke, AR (2015) Effects of laboratory colonization on Bactrocera dorsalis (Diptera, Tephritidae) mating behaviour: ‘what a difference a year makes’. ZooKeys 540, 369–383.CrossRefGoogle Scholar
Sciurano, RB, Segura, D, Rodriguero, M, Gómez Cendra, P, Allinghi, A, Cladera, JL and Vilardi, JC (2007) Sexual selection on multivariate phenotype in Anastrepha fraterculus (Diptera: Tephritidae) from Argentina. Florida Entomologist 90, 163–170.CrossRefGoogle Scholar
Segura, D, Petit-Marty, N, Sciurano, R, Vera, T, Calcagno, G, Allinghi, A, Gómez Cendra, P, Cladera, J and Vilardi, J (2007) Lekking behavior of Anastrepha fraterculus (Diptera: Tephritidae). Florida Entomologist 90, 154–162.CrossRefGoogle Scholar
Shelly, TE (2018 a) Larval host plant influences male body size and mating success in a tephritid fruit fly. Entomologia Experimentalis et Applicata 166, 41–52.CrossRefGoogle Scholar
Shelly, TE (2018 b) Sexual selection on leks: a fruit fly primer. Journal of Insect Science 18, 1–16.CrossRefGoogle ScholarPubMed
Shelly, TE and McInnis, DO (2016) and control of tephritid fruit flies: do species with complex courtship require higher overflooding ratios? Annals of the Entomological Society of America 109, 1–11.CrossRefGoogle Scholar
Shelly, TE and Nishimoto, J (2017) Does female mate choice confer direct fitness benefits? Results from a tephritid fruit fly. Annals of the Entomological Society of America 110, 204–211.Google Scholar
Tejeda, MT, Arredondo, J, Díaz-Fleischer, F and Pérez-Staples, D (2020) Does size matter? Mate choice in two lekking flies. Journal of Insect Science 20, 1–6.CrossRefGoogle ScholarPubMed
Webb, JC, Sivinski, J and Smittle, BJ (1987) Acoustical courtship signals and sexual success in irradiated Caribbean fruit flies (Anastrepha suspensa) (Diptera: Tephritidae). Florida Entomologist 70, 103–109.CrossRefGoogle Scholar
Weldon, C (2005) Mass-rearing and sterilisation alter mating behaviour of male Queensland fruit fly, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). Australian Journal of Entomology 44, 158–163.CrossRefGoogle Scholar
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