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

  • Celina B. Baines
  • Ilia Maria Ferzoco
  • Shannon J. McCauley
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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.

Keywords

Dispersal Sex-biased dispersal Intraspecific competition Sex ratio 
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Notes

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.

References

  1. Baines CB, McCauley SJ, Rowe L (2014) The interactive effects of competition and predation risk on dispersal in an insect. Biol Lett 10:20140287CrossRefPubMedPubMedCentralGoogle Scholar
  2. Baines CB, McCauley SJ, Rowe L (2015) Dispersal depends on body condition and predation risk in the semi-aquatic insect, Notonecta undulata. Ecol Evol ece3.1508Google Scholar
  3. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Soft 67:1–48CrossRefGoogle Scholar
  4. Bolnick DI, Otto SP (2013) The magnitude of local adaptation under genotype-dependent dispersal. Ecol Evol 3:4722–4735CrossRefPubMedPubMedCentralGoogle Scholar
  5. 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 87:290–312CrossRefPubMedGoogle Scholar
  6. Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80:205–225CrossRefPubMedGoogle Scholar
  7. 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 78:1234–1241CrossRefPubMedGoogle Scholar
  8. Brown JH, Kodric-Brown A (1977) Turnover rates in insular biogeography: effect of immigration on extinction. Ecology 58:445–449CrossRefGoogle Scholar
  9. 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 101:624–630CrossRefGoogle Scholar
  10. Clark LB (1928) Seasonal distribution and life history of Notonecta undulata in the Winnipeg Region, Canada. Ecology 9:383–403CrossRefGoogle Scholar
  11. 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 12:197–209CrossRefPubMedGoogle Scholar
  12. Clutton-Brock TH (1988) Reproductive success. University of Chicago Press, ChicagoGoogle Scholar
  13. Cote J, Fogarty S, Tymen B, Sih A, Brodin T (2013) Personality-dependent dispersal cancelled under predation risk. Proc R Soc Lond B Biol 280:20132349CrossRefGoogle Scholar
  14. Crnokrak P, Roff DA (1995) Fitness differences associated with calling behaviour in the two wing morphs of male sand crickets, Gryllus firmus. Anim Behav 50:1475–1481CrossRefGoogle Scholar
  15. Davis MA (1984) The flight and migration ecology of the red milkweed beetle (Tetraopes tetraophthalmus). Ecology 65:230–234CrossRefGoogle Scholar
  16. De Meester N, Bonte D (2010) Information use and density-dependent emigration in an agrobiont spider. Behav Ecol 21:992–998CrossRefGoogle Scholar
  17. Denno RF, Olmstead KL, McCloud ES (1989) Reproductive cost of flight capability: a comparison of life history traits in wing dimorphic planthoppers. Ecol Entomol 14:31–44CrossRefGoogle Scholar
  18. Doughty P, Sinervo B, Burghardt GM (1994) Sex-biased dispersal in a polygynous lizard, Uta stansburiana. Anim Behav 47:227–229CrossRefGoogle Scholar
  19. Edelaar P, Bolnick DI (2012) Non-random gene flow: an underappreciated force in evolution and ecology. Trends Ecol Evol 27:659–665CrossRefPubMedGoogle Scholar
  20. 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 264:127–132CrossRefGoogle Scholar
  21. 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 13:67–80CrossRefPubMedGoogle Scholar
  22. Fujisaki K (1992) A male fitness advantage to wing reduction in the oriental chinch bug, Cavelerius saccharivorus Okajima (Heteroptera: Lygaeidae). Res Popul Ecol 34:173–183CrossRefGoogle Scholar
  23. Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162CrossRefGoogle Scholar
  24. 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 219:226–233CrossRefGoogle Scholar
  25. 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 76:13–18CrossRefPubMedGoogle Scholar
  26. Guerra PA (2011) Evaluating the life-history trade-off between dispersal capability and reproduction in wing dimorphic insects: a meta-analysis. Biol Rev 86:813–835CrossRefPubMedGoogle Scholar
  27. Holekamp KE, Sherman PW (1989) Why male ground squirrels disperse: a multilevel analysis explains why only males leave home. Am Sci 77:232–239Google Scholar
  28. Holt RD, Gomulkiewicz R (1997) How does immigration influence local adaptation? A reexamination of a familiar paradigm. Am Nat 149:563–572CrossRefGoogle Scholar
  29. Hovestadt T, Mitesser O, Poethke H-J (2014) Gender-specific emigration decisions sensitive to local male and female density. Am Nat 184:38–51CrossRefPubMedGoogle Scholar
  30. Hungerford HB (1919) The biology and ecology of aquatic and semiaquatic Hemiptera. Kans Univ Sci Bull 11:3–334Google Scholar
  31. Hungerford HB (1933) The genus Notonecta of the world (Notonectidae-Hemiptera). Kans Univ Sci Bull 21:5–195Google Scholar
  32. Kerth G, Mayer F, Petit E (2002) Extreme sex-biased dispersal in the communally breeding, nonmigratory Bechstein’s bat (Myotis bechsteinii). Mol Ecol 11:1491–1498CrossRefPubMedGoogle Scholar
  33. Kuno E (1981) Dispersal and the persistence of populations in unstable habitats: a theoretical note. Oecologia 49:123–126CrossRefPubMedGoogle Scholar
  34. Lambin X (1994) Natal philopatry, competition for resources, and inbreeding avoidance in Townsend’s voles (Microtus townsendii). Ecology 75:224–235CrossRefGoogle Scholar
  35. Lawrence WS (1987) Dispersal: an alternative mating tactic conditional on sex ratio and body size. Behav Ecol Sociobiol 21:367–373CrossRefGoogle Scholar
  36. McCauley SJ (2010) Body size and social dominance influence breeding dispersal in male Pachydiplax longipennis (Odonata). Ecol Entomol 35:377–385CrossRefGoogle Scholar
  37. 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–E73CrossRefPubMedGoogle Scholar
  38. Mole S, Zera AJ (1993) Differential allocation of resources underlies the dispersal-reproduction trade-off in the wing-dimorphic cricket, Gryllus rubens. Oecologia 93:121–127CrossRefPubMedGoogle Scholar
  39. Odendaal FJ, Turchin P, Stermitz FR (1989) Influence of host-plant density and male harassment on the distribution of female Euphydryas anicia (Nymphalidae). Oecologia 78:283–288CrossRefPubMedGoogle Scholar
  40. Pasinelli G, Schiegg K, Walters JR (2004) Genetic and environmental influences on natal dispersal distance in a resident bird species. Am Nat 164:660–669CrossRefPubMedGoogle Scholar
  41. Perrin N, Mazalov V (2000) Local competition, inbreeding, and the evolution of sex-biased dispersal. Am Nat 155:116–127PubMedGoogle Scholar
  42. 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
  43. Roff DA (1984) The cost of being able to fly: a study of wing polymorphism in two species of crickets. Oecologia 63:30–37CrossRefPubMedGoogle Scholar
  44. Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 19:489–496CrossRefPubMedGoogle Scholar
  45. 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 59:1266–1277CrossRefGoogle Scholar
  46. 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 82:946–955CrossRefPubMedGoogle Scholar
  47. Van Dyck H, Baguette M (2005) Dispersal behaviour in fragmented landscapes: routine or special movements? Basic Appl Ecol 6:565–545Google Scholar
  48. Vignoli L, Vuerich V, Bologna MA (2012) Experimental study of dispersal behaviour in a wall lizard species (Podarcis sicula) (Sauria Lacertidae). Ethol Ecol Evol 24:244–256CrossRefGoogle Scholar
  49. Wade MJ, Goodnight CJ (1998) Perspective: the theories of Fisher and Wright in the context of metapopulations: when nature does many small experiments. Evolution 52:1537–1553CrossRefPubMedGoogle Scholar
  50. 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 60:373–381CrossRefGoogle Scholar
  51. Wild G, Taylor PD (2004) Kin selection models for the co-evolution of the sex ratio and sex-specific dispersal. Evol Ecol Res 6:481–502Google Scholar
  52. Zajitschek SRK, Zajitschek F, Brooks RC (2009) Demographic costs of inbreeding revealed by sex-specific genetic rescue effects. BMC Evol Biol 9:289CrossRefPubMedPubMedCentralGoogle Scholar
  53. Zera AJ (1984) Differences in survivorship, development rate and fertility between the long-winged and wingless morphs of the water strider, Limnoporus canaliculatus. Evolution 38:1023–1032CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Celina B. Baines
    • 1
    • 2
  • Ilia Maria Ferzoco
    • 1
  • Shannon J. McCauley
    • 1
    • 2
  1. 1.Biology DepartmentUniversity of Toronto MississaugaMississaugaCanada
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of TorontoTorontoCanada

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