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Females’ sequential mating decisions depend on both the quality of the courting male and the quality of the potential mates in a blood-sucking bug

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Abstract

This study investigates whether female sequential decisions on accepting or rejecting a courting male are based exclusively on the quality of the male present or are affected by the quality of potential mates. We used blood-sucking bugs Rhodnius prolixus as experimental subjects as females’ exhibit stereotyped discrimination behavior towards undesirable males, which allows sequential testing of a female’s preference for each male. We expect higher levels of female rejection when the benefit of finding a better quality male overrides the cost of rejecting a mating opportunity. Male quality was manipulated through changes in the feeding regime prior to the experiment because in this species nutritional condition affects males’ reproductive success. Females were simultaneously exposed to both a focal male currently available and a background male potentially available. The quality of each focal and background male could be either low or high and all the possible combinations were tested for each pair (low/high, high/low, high/high, low/low). We found that female rejection behavior depends not only on the quality of the focal male but also on the quality of the background male. This behavioral flexibility may allow females to maximize the benefits of their mating decisions.

Significance statement

Using an experimental approach, we study how females of a blood-sucking bug assess male quality and decide whether to accept or reject a mating opportunity in a sequential choice paradigm. Male quality (high/low) and male availability (current/potential) were manipulated. We show that female rejection depends on both the quality of the current and potential mates. Female rejection increases when better quality males are potentially available. This behavioral flexibility may allow females to maximize the benefits of mating decisions.

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References

  • Abdel-Azim MM, Aldosari SA, Shukla P (2018) Factors influencing mating behavior and success in the red palm weevil, Rhynchophorus ferrugineus Olivier (Coleoptera: Dryophthoridae). Neotrop Entomol. https://doi.org/10.1007/s13744-018-0592-9

  • Aluja M, Rull J, Sivinski J, Trujillo G, 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. J Insect Physiol 55:1091–1098

    Article  PubMed  CAS  Google Scholar 

  • Andersson MB (1994) Sexual selection. Princeton University Press, Princeton, New Jersey

    Google Scholar 

  • Andrade MCB, Mason AC (2000) Male condition, female choice, and extreme variation in repeated mating in a scaly cricket, Ornebius aperta (Orthoptera: Gryllidae: Mogoplistinae). J Insect Behav 13:483–497

    Article  Google Scholar 

  • Atwell A, Wagner WE (2014) Female mate choice plasticity is affected by the interaction between male density and female age in a field cricket. Anim Behav 98:177–183

    Article  Google Scholar 

  • Bakker TCM, Milinski M (1991) Sequential female choice and the previous male effect in sticklebacks. Behav Ecol Sociobiol 29:205–210

    Article  Google Scholar 

  • Bateman PW, Gilson LN, Ferguson JWH (2001) Male size and sequential mate preference in the cricket Gryllus bimaculatus. Anim Behav 61:631–637

    Article  Google Scholar 

  • Berglund A (1995) Many mates make male pipefish choosy. Behaviour 131:213–218

    Article  Google Scholar 

  • Berglund A, Widemo MS, Rosenqvist G (2005) Sex-role reversal revisited: choosy females and ornamented, competitive males in a pipefish. Behav Ecol 16:649–655

    Article  Google Scholar 

  • Bleu J, Bessa-Gomes C, Laloia D (2012) Evolution of female choosiness and mating frequency: effects of mating cost, density and sex ratio. Anim Behav 83:131–136

    Article  Google Scholar 

  • Bonduriansky R (2001) The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biol Rev 76:305–339

    Article  PubMed  CAS  Google Scholar 

  • Bonduriansky R, Mallet MA, Arbuthnott D, Pawlowsky-Glahn V, Egozcue JJ, Rundle HD (2015) Differential effects of genetic vs. environmental quality in Drosophila melanogaster suggest multiple forms of condition dependence. Ecol Lett. https://doi.org/10.1111/ele.12412

  • Cardoso Giaquinto P, da Silva Berbert CM, Delicio HC (2010) Female preferences based on male nutritional chemical traits. Behav Ecol Sociobiol 64:1029–1035

    Article  Google Scholar 

  • Cotton S, Fowler K, Pomiankowski A (2004) Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proc R Soc Lond B 271:771–783

    Article  Google Scholar 

  • Crespo JG, Manrique G (2007) Mating behavior of the haematophagous bug Triatoma infestans: role of Brindley’s and metasternal glands. J Insect Physiol 53:708–714

    Article  PubMed  CAS  Google Scholar 

  • Crowley PH, Travers SE, Linton MC, Cohn SL, Sih A, Craig Sargent R (1991) Mate density, predation risk, and the seasonal sequence of mate choices: a dynamic game. Am Nat 137:567–596

    Article  Google Scholar 

  • De Simone GA (2018) Factores y reglas de decisión involucrados en la elección de pareja sexual en el insecto hematófago Rhodnius prolixus (Hemiptera: Reduviidae). Dissertation (Ph D. Thesis), Universidad de Buenos Aires

  • Fricke C, Bretman A, Chapman T (2008) Adult male nutrition and reproductive success in Drosophila melanogaster. Evolution 62:3170–3177

    Article  PubMed  Google Scholar 

  • Friend W, Choy C, Cartwright E (1965) The effect of nutrient intake on the development and the egg production of Rhodnius prolixus Stål (Hemiptera: Reduviidae). Can J Zool 43:891–904

    Article  PubMed  CAS  Google Scholar 

  • Gabor CR, Halliday TR (1997) Sequential mate choice by multiply mating smooth newts: females become more choosy. Behav Ecol 8:162–166

    Article  Google Scholar 

  • Goodchild AJP (1955) Some observations on growth and egg production of the blood-sucking Reduviids, Rhodnius prolixus and Triatoma infestans. Physiol Entomol 30:137–144

    Google Scholar 

  • Griggio M, Hoi H, Lukasch B, Pilastro A (2016) Context-dependent female preference for multiple ornaments in the bearded reedling. Ecol Evol 6:493–501

    Article  PubMed  PubMed Central  Google Scholar 

  • Hebets EA (2003) Subadult experience influences adult mate choice in an arthropod: exposed female wolf spiders prefer males of a familiar phenotype. PNAS 100:13393

    Article  CAS  Google Scholar 

  • Janetos AC (1980) Strategies of female mate choice: a theoretical analysis. Behav Ecol Sociobiol 7:107–112

    Article  Google Scholar 

  • Jennions MD, Petrie M (1997) Variation in mate choice and mating preferences: a review of causes and consequences. Biol Rev 72:283–327

    Article  PubMed  CAS  Google Scholar 

  • Kahrl AF, Cox RM (2015) Diet affects ejaculate traits in a lizard with condition-dependent fertilization success. Behav Ecol 26:1502–1511

    Article  Google Scholar 

  • Khalifa A (1950) Spermatophore production and egg-laying behaviour in Rhodnius prolixus Stål (Hemiptera; Reduviidae). Parasitology 40:283–289

    Article  PubMed  CAS  Google Scholar 

  • Kudo H, Karino K (2012) Short-term change in male sexually selected traits and female mate preference in the guppy Poecilia reticulate. Ichthyol Res 59:1–7

    Article  Google Scholar 

  • Lazzari CR (1992) Circadian organization of locomotion activity in the haematophagous bug Triatoma infestans. J Insect Physiol 38:895–903

    Article  Google Scholar 

  • Locatello L, Poli F, Rasotto MB (2015) Context-dependent evaluation of prospective mates in a fish. Behav Ecol Sociobiol 69:1119–1126

    Article  PubMed  PubMed Central  Google Scholar 

  • Manrique G, Lazzari CR (1994) Sexual behaviour and stridulation during mating in Triatoma infestans (Hemiptera: Reduviidae). Mem Inst Oswaldo Cruz 89:629–633

    Article  PubMed  CAS  Google Scholar 

  • Manrique G, Lazzari CR (1995) Existence of a sex pheromone in Triatoma infestans (Hemiptera: Reduviidae): I. Behavioural evidences. Mem Inst Oswaldo Cruz 90:645–648

    Article  PubMed  CAS  Google Scholar 

  • Manrique G, Vitta ACR, Ferreira RA, Zani CL, Unelius CR, Lazzari CR, Diotaiuti L, Lorenzo MG (2006) Chemical communication in Chagas disease vectors. Source, identity and potential function of volatiles released by the metasternal and Brindley’s glands of Triatoma infestans adults. J Chem Ecol 32:2035–2052

    Article  PubMed  CAS  Google Scholar 

  • Murphy CG, Gerhardt HC (2002) Mate sampling by female barking treefrogs (Hyla gratiosa). Behav Ecol 13:472–480

    Article  Google Scholar 

  • Neelon DP, Höbel G (2017) Social plasticity in choosiness in green tree frogs, Hyla cinerea. Behav Ecol 28:1540–1546

    Article  Google Scholar 

  • Pires HHR, Lorenzo MG, Lazzari CR, Diotaiuti L, Manrique G (2004) The sexual behaviour of Panstrongylus megistus (Hemiptera: Reduviidae): an experimental study. Mem Inst Oswaldo Cruz 99:295–300

    Article  PubMed  Google Scholar 

  • Pitcher TE, Neff BD, Rodd FH, Locke R (2003) Multiple mating and sequential mate choice in guppies: females trade up. Proc R Soc B Biol Sci 270:1623–1629. https://doi.org/10.1098/rspb.2002.2280

    Article  Google Scholar 

  • Pompilio L, González Franco M, Chisari LB, Manrique G (2016) Female choosiness and mating opportunities in the blood-sucking bug Rhodnius prolixus. Behaviour 153:1863–1878

    Article  Google Scholar 

  • Pontes GB, Lorenzo MG (2012) Female metasternal gland odours mediate male aggregation in Rhodnius prolixus, a triatomid bug. Med Vet Entomol 26:33–36

    Article  PubMed  CAS  Google Scholar 

  • Poulin R, Vickery WL (1996) Parasite-mediated sexual selection: just how choosy are parasitized females? Behav Ecol Sociobiol 38:43–49

    Article  Google Scholar 

  • Real LA (1990) Search theory and mate choice. I. Models of single-sex discrimination. Am Nat 136:376–405

    Article  Google Scholar 

  • Real LA (1991) Animal choice behavior and the evolution of cognitive architecture. Science 253:980–986

    Article  PubMed  CAS  Google Scholar 

  • Reaney T (2009) Female preference for male phenotypic traits in a fiddler crab: do females use absolute or comparative evaluation? Anim Behav 7:139–143

    Article  Google Scholar 

  • Roces F, Manrique G (1996) Different stridulatory vibrations during sexual behaviour and disturbance in the blood-sucking bug Triatoma infestans (Hemiptera: Reduviidae). J Insect Physiol 42:231–238

    Article  CAS  Google Scholar 

  • Schäfer MA, Uhl G (2005) Sequential mate encounters: female but not male body size influences female remating behavior. Behav Ecol 16:461–466

    Article  Google Scholar 

  • Shelly TE, Bailey WJ (1992) Experimental manipulation of mate choice by male katydids: the effect of female encounter rate. Behav Ecol Sociobiol 30:277–282

    Article  Google Scholar 

  • Vitta ACR, Lorenzo MG (2009) Copulation and mate guarding behavior in Triatoma brasiliensis (Hemiptera: Reduviidae). J Med Entomol 46:789–795

    Article  PubMed  Google Scholar 

  • Wagner WE Jr, Smeds MR, Wiegmann DD (2001) Experience affects female responses to male song in the variable field cricket Gryllus lineaticeps (Orthoptera, Gryllidae). Ethol 107:769–776

    Article  Google Scholar 

  • Wiegmann DD, Angeloni LM, Seubert SM, Wade JG (2013) Mate choice decisions by searchers. Curr Zool 59:184–199

    Article  Google Scholar 

  • Willis PM, Ryan MJ, Rosenthal GG (2011) Encounter rates with conspecific males influence female mate choice in a naturally hybridizing fish. Behav Ecol 22:1234–1240

    Article  Google Scholar 

  • Wittenberger JF (1983) Tactics of mate choice. In: Bateson P (ed) Mate choice. Cambridge University Press, New York, pp 435–447

    Google Scholar 

  • Xie J, De Clercq P, Zhang Y, Wu H, Pan C, Pangb H (2015) Nutrition-dependent phenotypes affect sexual selection in a ladybird. Sci Rep 7:159–170

    Google Scholar 

  • Zahavi A (1975) Mate selection-a selection for a handicap. J Theor Biol 53:205–214

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Dr. Gerardo Cueto, Facultad de Ciencias Exactas y Naturales, Departamento de Ecología Genética y Evolución and IEGEBA, CONICET-UBA, Universidad de Buenos Aires, for statistical advice.

Funding

This work was supported by Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Departamento de Biodiversidad y Biología Experimental, Programación Científica 2014-2017 (20020130100341BA).

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Author notes

  1. Gabriel Manrique and Lorena Pompilio contributed equally to this work.

Authors and Affiliations

  1. Laboratorio de Fisiología de Insectos, Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Instituto de Biodiversidad y Biología Experimental y Aplicada, IBBEA, CONICET-UBA, Ciudad Universitaria, Pabellón II, C1428EHA, Buenos Aires, Argentina

    Gabriel A. De Simone & Gabriel Manrique

  2. Laboratorio de Ecología y Comportamiento Animal, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, IEGEBA, CONICET-UBA, Ciudad Universitaria, Pabellón II, C1428EHA, Buenos Aires, Argentina

    Lorena Pompilio

Authors
  1. Gabriel A. De Simone
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  2. Gabriel Manrique
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  3. Lorena Pompilio
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Correspondence to Gabriel Manrique or Lorena Pompilio.

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The authors declare that they have no conflict of interest.

Ethical approval

We did not observe any harmful effects associated to our experimental manipulation. At the end of the experiment, the insects were returned to their breeding cages and the hens to the chicken coop. All animals were handled according to the biosafety rules from the Servicio de Higiene y Seguridad of the Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Argentina.

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Communicated by S. Sakaluk

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De Simone, G.A., Manrique, G. & Pompilio, L. Females’ sequential mating decisions depend on both the quality of the courting male and the quality of the potential mates in a blood-sucking bug. Behav Ecol Sociobiol 72, 145 (2018). https://doi.org/10.1007/s00265-018-2560-0

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