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Sex-biased dispersal is independent of sex ratio in a semiaquatic insect

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Abstract

Dispersal influences a variety of ecological and evolutionary dynamics including metapopulation persistence and local adaptation. Sex-biased dispersal evolves when the costs and benefits associated with dispersal differ between the sexes. These costs and benefits may be fixed, resulting in a consistent pattern of sex-biased dispersal within species whereby one sex always disperses more and/or further than the other. Alternatively, the costs and benefits may vary depending on the intensity of competition experienced by the two sexes. In this case, the direction of the sex bias may be plastic and depend on the sex ratio of the population. In the current study, we asked whether a semiaquatic, flight capable insect (Notonecta undulata) exhibits sex-biased dispersal and whether the strength of intrasexual competition experienced by males and females determines the direction of the sex bias. We conducted a mesocosm experiment in which we manipulated the population sex ratio and measured the probability of dispersal for males and females. We found that while both sexes dispersed, male dispersal rates were higher, and this pattern was independent of sex ratio. This suggests that fixed sex-specific dispersal costs and/or benefits are likely to be more important determinants of sex-biased dispersal in notonectids than population sex ratio.

Significance statement

Dispersal is the process by which individuals move through space and cause gene flow and therefore is a major factor determining the distribution of individuals, populations, species, and alleles—a topic which is one of the core themes in ecology. Dispersers commonly differ from non-dispersers in a variety of phenotypes, including sex. Sex-biased dispersal may have important implications for the populations that send out and receive dispersers, because males and females have different impacts on populations. We explored whether sex-specific dispersal behavior in an insect (Notonecta undulata) changes depending on how intensely individuals have to compete for resources (e.g., food, mates) with individuals of the same sex. We found that males dispersed more, and this was true regardless of which sex experienced stronger intrasexual competition. This suggests that males experience lower costs and/or greater benefits from dispersing than do females.

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References

  • Baines CB, McCauley SJ, Rowe L (2014) The interactive effects of competition and predation risk on dispersal in an insect. Biol Lett 10:20140287

    Article  PubMed  PubMed Central  Google Scholar 

  • Baines CB, McCauley SJ, Rowe L (2015) Dispersal depends on body condition and predation risk in the semi-aquatic insect, Notonecta undulata. Ecol Evol ece3.1508

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Soft 67:1–48

    Article  Google Scholar 

  • Bolnick DI, Otto SP (2013) The magnitude of local adaptation under genotype-dependent dispersal. Ecol Evol 3:4722–4735

    Article  PubMed  PubMed Central  Google Scholar 

  • Bonte D, Van Dyck H, Bullock JM, Coulon A, Delgado M, Gibbs M, Lehouck V, Matthysen E, Mustin K, Saastamoinen M, Schtickzelle N, Stevens VM, Vandewoestijne S, Baguette M, Barton K, Benton TG, Chaput-Bardy A, Clobert J, Dytham C, Hovestadt T, Meier CM, Palmer SC, Turlure C, Travis JM (2012) Costs of dispersal. Biol Rev 87:290–312

    Article  PubMed  Google Scholar 

  • Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80:205–225

    Article  PubMed  Google Scholar 

  • Bowler DE, Benton TG (2009) Variation in dispersal mortality and dispersal propensity among individuals: the effects of age, sex and resource availability. J Anim Ecol 78:1234–1241

    Article  PubMed  Google Scholar 

  • Brown JH, Kodric-Brown A (1977) Turnover rates in insular biogeography: effect of immigration on extinction. Ecology 58:445–449

    Article  Google Scholar 

  • Caudill CC (2003) Measuring dispersal in a metapopulation using stable isotope enrichment: high rates of sex-biased dispersal between patches in a mayfly population. Oikos 101:624–630

    Article  Google Scholar 

  • Clark LB (1928) Seasonal distribution and life history of Notonecta undulata in the Winnipeg Region, Canada. Ecology 9:383–403

    Article  Google Scholar 

  • Clobert J, Le Galliard JF, Cote J, Meylan S, Massot M (2009) Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecol Lett 12:197–209

    Article  PubMed  Google Scholar 

  • Clutton-Brock TH (1988) Reproductive success. University of Chicago Press, Chicago

    Google Scholar 

  • Cote J, Fogarty S, Tymen B, Sih A, Brodin T (2013) Personality-dependent dispersal cancelled under predation risk. Proc R Soc Lond B Biol 280:20132349

    Article  Google Scholar 

  • Crnokrak P, Roff DA (1995) Fitness differences associated with calling behaviour in the two wing morphs of male sand crickets, Gryllus firmus. Anim Behav 50:1475–1481

    Article  Google Scholar 

  • Davis MA (1984) The flight and migration ecology of the red milkweed beetle (Tetraopes tetraophthalmus). Ecology 65:230–234

    Article  Google Scholar 

  • De Meester N, Bonte D (2010) Information use and density-dependent emigration in an agrobiont spider. Behav Ecol 21:992–998

    Article  Google Scholar 

  • Denno RF, Olmstead KL, McCloud ES (1989) Reproductive cost of flight capability: a comparison of life history traits in wing dimorphic planthoppers. Ecol Entomol 14:31–44

    Article  Google Scholar 

  • Doughty P, Sinervo B, Burghardt GM (1994) Sex-biased dispersal in a polygynous lizard, Uta stansburiana. Anim Behav 47:227–229

    Article  Google Scholar 

  • Edelaar P, Bolnick DI (2012) Non-random gene flow: an underappreciated force in evolution and ecology. Trends Ecol Evol 27:659–665

    Article  PubMed  Google Scholar 

  • Favre L, Balloux F, Goudet J, Perrin N (1997) Female-biased dispersal in the monogamous mammal Crocidura russula: evidence from field data and microsatellite patterns. Proc R Soc Lond Biol 264:127–132

    Article  CAS  Google Scholar 

  • Fraser DJ, Lippe C, Bernatchez L (2004) Consequences of unequal population size, asymmetric gene flow and sex-biased dispersal on population structure in brook charr (Salvelinus fontinalis). Mol Ecol 13:67–80

    Article  CAS  PubMed  Google Scholar 

  • Fujisaki K (1992) A male fitness advantage to wing reduction in the oriental chinch bug, Cavelerius saccharivorus Okajima (Heteroptera: Lygaeidae). Res Popul Ecol 34:173–183

    Article  Google Scholar 

  • Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162

    Article  Google Scholar 

  • Gros A, Hovestadt T, Poethke HJ (2008) Evolution of sex-biased dispersal: the role of sex-specific dispersal costs, demographic stochasticity, and inbreeding. Ecol Model 219:226–233

    Article  Google Scholar 

  • Gros A, Poethke HJ, Hovestadt T (2009) Sex-specific spatio-temporal variability in reproductive success promotes the evolution of sex-biased dispersal. Theor Popul Biol 76:13–18

    Article  PubMed  Google Scholar 

  • Guerra PA (2011) Evaluating the life-history trade-off between dispersal capability and reproduction in wing dimorphic insects: a meta-analysis. Biol Rev 86:813–835

    Article  PubMed  Google Scholar 

  • Holekamp KE, Sherman PW (1989) Why male ground squirrels disperse: a multilevel analysis explains why only males leave home. Am Sci 77:232–239

    Google Scholar 

  • Holt RD, Gomulkiewicz R (1997) How does immigration influence local adaptation? A reexamination of a familiar paradigm. Am Nat 149:563–572

    Article  Google Scholar 

  • Hovestadt T, Mitesser O, Poethke H-J (2014) Gender-specific emigration decisions sensitive to local male and female density. Am Nat 184:38–51

    Article  PubMed  Google Scholar 

  • Hungerford HB (1919) The biology and ecology of aquatic and semiaquatic Hemiptera. Kans Univ Sci Bull 11:3–334

    Google Scholar 

  • Hungerford HB (1933) The genus Notonecta of the world (Notonectidae-Hemiptera). Kans Univ Sci Bull 21:5–195

    Google Scholar 

  • Kerth G, Mayer F, Petit E (2002) Extreme sex-biased dispersal in the communally breeding, nonmigratory Bechstein’s bat (Myotis bechsteinii). Mol Ecol 11:1491–1498

    Article  CAS  PubMed  Google Scholar 

  • Kuno E (1981) Dispersal and the persistence of populations in unstable habitats: a theoretical note. Oecologia 49:123–126

    Article  PubMed  Google Scholar 

  • Lambin X (1994) Natal philopatry, competition for resources, and inbreeding avoidance in Townsend’s voles (Microtus townsendii). Ecology 75:224–235

    Article  Google Scholar 

  • Lawrence WS (1987) Dispersal: an alternative mating tactic conditional on sex ratio and body size. Behav Ecol Sociobiol 21:367–373

    Article  Google Scholar 

  • McCauley SJ (2010) Body size and social dominance influence breeding dispersal in male Pachydiplax longipennis (Odonata). Ecol Entomol 35:377–385

    Article  Google Scholar 

  • McCauley SJ, Brodin T, Hammond J (2010) Foraging rates of larval dragonfly colonists are positively related to habitat isolation: results from a landscape-level experiment. Am Nat 175:E66–E73

    Article  PubMed  Google Scholar 

  • Mole S, Zera AJ (1993) Differential allocation of resources underlies the dispersal-reproduction trade-off in the wing-dimorphic cricket, Gryllus rubens. Oecologia 93:121–127

    Article  PubMed  Google Scholar 

  • Odendaal FJ, Turchin P, Stermitz FR (1989) Influence of host-plant density and male harassment on the distribution of female Euphydryas anicia (Nymphalidae). Oecologia 78:283–288

    Article  CAS  PubMed  Google Scholar 

  • Pasinelli G, Schiegg K, Walters JR (2004) Genetic and environmental influences on natal dispersal distance in a resident bird species. Am Nat 164:660–669

    Article  PubMed  Google Scholar 

  • Perrin N, Mazalov V (2000) Local competition, inbreeding, and the evolution of sex-biased dispersal. Am Nat 155:116–127

    CAS  PubMed  Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical computing, version 3.1.1. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org

  • Roff DA (1984) The cost of being able to fly: a study of wing polymorphism in two species of crickets. Oecologia 63:30–37

    Article  PubMed  Google Scholar 

  • Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 19:489–496

    Article  PubMed  Google Scholar 

  • Therry L, Lefevre E, Bonte D, Stoks R (2014) Increased activity and growth rate in the non-dispersive aquatic larval stage of a damselfly at an expanding range edge. Freshw Biol 59:1266–1277

    Article  Google Scholar 

  • Trochet A, Legrand D, Larranga N, Ducatez S, Calvez O, Cote J, Clobert J, Baguette M (2013) Population sex ratio and dispersal in experimental, two-patch metapopulations of butterflies. J Anim Ecol 82:946–955

    Article  PubMed  Google Scholar 

  • Van Dyck H, Baguette M (2005) Dispersal behaviour in fragmented landscapes: routine or special movements? Basic Appl Ecol 6:565–545

    Google Scholar 

  • Vignoli L, Vuerich V, Bologna MA (2012) Experimental study of dispersal behaviour in a wall lizard species (Podarcis sicula) (Sauria Lacertidae). Ethol Ecol Evol 24:244–256

    Article  Google Scholar 

  • Wade MJ, Goodnight CJ (1998) Perspective: the theories of Fisher and Wright in the context of metapopulations: when nature does many small experiments. Evolution 52:1537–1553

    Article  PubMed  Google Scholar 

  • Wiklund C, Forsberg J (1991) Sexual size dimorphism in relation to female polygamy and protandry in butterflies: a comparative study of Swedish Pieridae and Satyridae. Oikos 60:373–381

    Article  Google Scholar 

  • Wild G, Taylor PD (2004) Kin selection models for the co-evolution of the sex ratio and sex-specific dispersal. Evol Ecol Res 6:481–502

    Google Scholar 

  • Zajitschek SRK, Zajitschek F, Brooks RC (2009) Demographic costs of inbreeding revealed by sex-specific genetic rescue effects. BMC Evol Biol 9:289

    Article  PubMed  PubMed Central  Google Scholar 

  • Zera AJ (1984) Differences in survivorship, development rate and fertility between the long-winged and wingless morphs of the water strider, Limnoporus canaliculatus. Evolution 38:1023–1032

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank John Stinchcombe and Stephan Schneider at the Koffler Scientific Reserve for logistical support and for allowing us to use the site. We also thank the Nature Conservancy of Canada for allowing us to collect animals at the Happy Valley Forest site (permit no.: AG-ON-2016-150619). Comments from students in the McCauley Lab at the University of Toronto Mississauga improved this manuscript. Funding was provided by a University of Toronto Fellowship and a National Science and Engineering Research Council Postgraduate Scholarship awarded to CBB, a Koffler Scientific Reserve Undergraduate Student Research Award to IMF, and a grant to SJM from the National Science and Engineering Research Council Discovery Grant program.

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Correspondence to Celina B. Baines.

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Communicated by S. Sakaluk

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Baines, C.B., Ferzoco, I.M. & McCauley, S.J. Sex-biased dispersal is independent of sex ratio in a semiaquatic insect. Behav Ecol Sociobiol 71, 119 (2017). https://doi.org/10.1007/s00265-017-2348-7

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