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Sex-dependent personality in two invasive species of mosquitofish

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Abstract

A key challenge in invasion biology is identifying characteristics that allow some species to be repeatedly successful at invading novel environments. Invasions can often be disproportionately driven by a single sex, with differences in behavioural mechanisms between the sexes potentially underlying sex-biased invasiveness. Here, we took an animal personality approach to study the behaviour of two repeatedly successful congeneric invasive species, the western mosquitofish, Gambusia affinis, and the eastern mosquitofish, Gambusia holbrooki. In each species, we investigated whether males and females shared common personality traits (i.e. behavioural types and behavioural syndromes), with the aim of identifying possible behavioural mechanisms that could help explain why mosquitofish invasions are often characterised by sex-biased founder populations. We found sex-dependent personality, although sex differences varied between species. Male G. affinis were bolder and less social than female G. affinis, whereas we found no behavioural type differences between the sexes in G. holbrooki. We also found a consistent correlation between boldness and exploration in both sexes within G. affinis, but this correlation was weak in G. holbrooki. Finally, exploration was also correlated with sociability in male G. affinis, but not in females. Our results suggest that behavioural tendencies may diverge, both among species and between the sexes, because of adaptation experienced during different invasion pathways. Broadly, identifying the behavioural mechanisms that predict an individual’s ‘invasiveness’ may be difficult to tease apart between species because each invasion is characterised by different abiotic and biotic interactions that likely require different suites of behaviours. Future studies are needed to elucidate whether, in fact, personality variation between the sexes can mediate the occurrence of sex-biased invasions.

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References

  • Aplin LM, Farine DR, Morand-Ferron J, Cockburn A, Thornton A, Sheldon BC (2015) Experimentally induced innovations lead to persistent culture via conformity in wild birds. Nature 518:538

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Bell AM, Sih A (2007) Exposure to predation generates personality in three-spined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834

    Article  PubMed  Google Scholar 

  • Bertram MG, Saaristo M, Martin JM, Ecker TE, Michelangeli M, Johnstone CP, Wong BBM (2018) Field-realistic exposure to the androgenic endocrine disruptor 17β-trenbolone alters ecologically important behaviours in female fish across multiple contexts. Environ Pollut 243:900–911

    Article  CAS  PubMed  Google Scholar 

  • Bevan PA, Gosetto I, Jenkins ER, Barnes I, Ioannou CC (2018) Regulation between personality traits: individual social tendencies modulate whether boldness and leadership are correlated. Proc R Soc B Biol Sci 285:20180829

    Article  Google Scholar 

  • Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends Ecol Evol 23:361–368

    Article  PubMed  Google Scholar 

  • Biro PA, Adriaenssens B, Sampson P (2014) Individual and sex-specific differences in intrinsic growth rate covary with consistent individual differences in behaviour. J Anim Ecol 83:1186–1195

    Article  PubMed  Google Scholar 

  • Blackburn TM, Duncan RP (2001) Establishment patterns of exotic birds are constrained by non-random patterns in introduction. J Biogeogr 28:927–939

    Article  Google Scholar 

  • Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135

    Article  PubMed  Google Scholar 

  • Briski E, Chan FT, Darling JA, Lauringson V, MacIsaac HJ, Zhan A, Bailey SA (2018) Beyond propagule pressue: importance of selection during the transport stage of biological invasions. Front Ecol Environ 16:345–353

    Article  PubMed  PubMed Central  Google Scholar 

  • Britton RH, Moser ME (1982) Size specific predation by herons and its effect on the sex-ratio of natural populations of the mosquito fish Gambusia affinis. Oecologia 53:146–151

    Article  PubMed  Google Scholar 

  • Chapple DG, Wong BBM (2016) The role of behavioural variation across different stages of the introduction process. Chapter 2. In: Weis JS, Sol D (eds) Biological invasions and animal behaviour. Cambridge University Press, Cambridge, pp 7–25

    Chapter  Google Scholar 

  • Chapple DG, Simmonds SM, Wong BBM (2012) Can behavioral and personality traits influence the success of unintentional species introductions? Trends Ecol Evol 27:57–64

    Article  PubMed  Google Scholar 

  • Conover WJ, Johnson ME, Johnson MM (1981) A comparative study of tests forhomogeneity of variances, with applications to the outer continental shelf bidding data. Technometrics 23:351–361

    Article  Google Scholar 

  • Cote J, Clobert J, Brodin T, Fogarty S, Sih A (2010a) Personality-dependent dispersal: characterization, ontogeny and consequences for spatially structured populations. Philos Trans R Soc Biol Sci 365:4065–4076

    Article  CAS  Google Scholar 

  • Cote J, Fogarty S, Weinersmith K, Brodin T, Sih A (2010b) Personality traits and dispersal tendency in the invasive mosquitofish (Gambusia affinis). Proc R Soc Biol Sci 277:1571–1579

    Article  Google Scholar 

  • Cote J, Fogarty S, Brodin T, Weinersmith K, Sih A (2011) Personality-dependent dispersal in the invasive mosquitofish: group composition matters. Proc R Soc Biol Sci 278:1670–1678

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Cote J, Brodin T, Fogarty S, Sih A (2017) Non-random dispersal mediates invader impacts on the invertebrate community. J Anim Ecol 86:1298–1307

    Article  PubMed  Google Scholar 

  • Debecker S, Sanmartín-Villar I, de Guinea-Luengo M, Cordero-Rivera A, Stoks R (2016) Integrating the pace-of-life syndrome across species, sexes and individuals: covariation of life history and personality under pesticide exposure. J Anim Ecol 85:726–738

    Article  PubMed  Google Scholar 

  • Dingemanse NJ, Wright J, Kazem AJ, Thomas DK, Hickling R, Dawnay N (2007) Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76:1128–1138

    Article  PubMed  Google Scholar 

  • Duckworth RA, Badyaev AV (2007) Coupling dispersal and aggression facilitates the rapid range expansion of a passerine bird. Proc Natl Acad Sci USA 104:15017–15022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fairbairn DJ, Blanckenhorn WU, Székely T (2007) Sex, size, and gender roles: evolutionary studies of sexual size dimorphism. Oxford University Press, Oxford

    Book  Google Scholar 

  • Felden A, Paris CI, Chapple DG, Haywood J, Suarez AV, Tsutsui ND, Lester PJ, Gruber MAM (2018) Behavioural variation and plasticity along an invasive ant introduction pathway. J Anim Ecol 87:1653–1666

    Article  PubMed  Google Scholar 

  • Fogarty S, Cote J, Sih A (2011) Social personality polymorphism and the spread of invasive species: a model. Am Nat 177:273–287

    Article  PubMed  Google Scholar 

  • Foster WA, Treherne JE (1981) Evidence for the dilution effect in the selfish herd from fish predation on a marine insect. Nature 293:466–467

    Article  Google Scholar 

  • Fryxell DC, Arnett HA, Apgar TM, Kinnison MT, Palkovacs EP (2015) Sex ratio variation shapes the ecological effects of a globally introduced freshwater fish. Proc R Soc B 282:2051970

    Article  CAS  Google Scholar 

  • Gómez-Laplaza LM, Morgan EE (2000) Laboratory studies of the effects of short-term isolation on aggressive behaviour in fish. Mar Freshw Behav Physiol 33:63–102

    Article  Google Scholar 

  • Gruber J, Brown G, Whiting MJ, Shine R (2017) Geographic divergence in dispersal-related behaviour in cane toads from range-front versus range-core populations in Australia. Behav Ecol Sociobiol 71:38

    Article  Google Scholar 

  • Gutowsky LFG, Fox MG (2011) Occupation, body size and sex ratio of round goby (Neogobius melanostomus) in established and newly invaded areas of an Ontario river. Hydrobiologia 671:27–35

    Article  Google Scholar 

  • Harris S, Ramnarine IW, Smith HG, Pettersson LB (2010) Picking personalities apart: estimating the influence of predation, sex and body size on boldness in the guppy Poecilia reticulata. Oikos 119:1711–1718

    Article  Google Scholar 

  • Heinen-Kay JL, Schmidt DA, Stafford AT, Costa MT, Peterson MN, Kern EM, Langerhan BR (2016) Predicting multifarious behavioural divergence in the wild. Anim Behav 121:3–10

    Article  Google Scholar 

  • Hoare D, Krause J, Peuhkuri N, Godin JG (2000) Body size and shoaling in fish. J Fish Biol 57:1351–1366

    Article  Google Scholar 

  • Holway DA, Suarez AV (1999) Animal behavior: an essential component of invasion biology. Trends Ecol Evol 14:328–330

    Article  CAS  PubMed  Google Scholar 

  • Hulthén K, Chapman BB, Nilsson PA, Hansson LA, Skov C, Brodersen J, Vinterstare J, Brönmark C (2017) A predation cost to bold fish in the wild. Sci Rep 7:1239

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Juette T, Cucherousset J, Cote J (2014) Animal personality and the ecological impacts of freshwater non-native species. Curr Zool 60:417–427

    Article  Google Scholar 

  • King AJ, Fürtbauer I, Mamuneas D, James C, Manica A (2013) Sex-differences and temporal consistency in stickleback fish boldness. PLoS ONE 8:e81116

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Llewelyn J, Phillips BL, Alford RA, Schwarzkopf L, Shine R (2010) Locomotor performance in an invasive species: cane toads from the invasion front have greater endurance, but not speed, compared to conspecifics from a long-colonised area. Oecologia 162:343–348

    Article  PubMed  Google Scholar 

  • Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the world’s worst invasive alien species: a selection from the Global Invasive Species Database, 2nd edn. The Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN)

  • Marentette JR, Wang G, Tong S, Sopinka NM, Taves MD, Koops MA, Balshine S (2011) Laboratory and field evidence of sex-biased movement in the invasive round goby. Behav Ecol Sociobiol 65:2239–2249

    Article  Google Scholar 

  • Martín J, López P, Cooper WE Jr (2003) Lost of mating opportunities influences refuge use in the Iberian rock lizard, Lacerta monticola. Behav Ecol Sociobiol 54:505–510

    Article  Google Scholar 

  • McPeek MA (1992) Mechanisms of sexual selection operating on body size in the mosquitofish (Gambusia holbrooki). Behav Ecol 3:1–12

    Article  Google Scholar 

  • Mennen GJ, Laskowski KL (2018) Defence is the best offence: invasive prey behaviour is more important than native predator behaviour. Anim Behav 138:157–164

    Article  Google Scholar 

  • Michelangeli M, Wong BBM, Chapple DG (2016a) It’s a trap: sampling bias due to animal personality is not always inevitable. Behav Ecol 27:62–67

    Article  Google Scholar 

  • Michelangeli M, Chapple DG, Wong BBM (2016b) Are behavioural syndromes sex specific? Personality in a widespread lizard species. Behav Ecol Sociobiol 70:1911–1919

    Article  Google Scholar 

  • Michelangeli M, Smith CR, Wong BBM, Chapple DG (2017) Aggression mediates dispersal tendency in an invasive lizard. Anim Behav 133:29–34

    Article  Google Scholar 

  • Michelangeli M, Goulet CG, Kang HS, Wong BBM, Chapple DG (2018a) Integrating thermal physiology within a syndrome: locomotion, personality and habitat selection in an ectotherm. Funct Ecol 32:970–981

    Article  Google Scholar 

  • Michelangeli M, Chapple DG, Goulet CG, Bertram MG, Wong BBM (2018b) Behavioural syndromes vary among geographically distinct populations in a reptile. Behav Ecol 30:393–401

    Article  Google Scholar 

  • Miller TE, Inouye BD (2013) Sex and stochasticity affect range expansion of experimental invasions. Ecol Lett 16:354–361

    Article  PubMed  Google Scholar 

  • Mishra A, Tung S, Shreenidhi PM, Aamir Sadiq MA, Shree Struti VR, Chakraborty PP, Dey S (2018) Sex differences in dispersal syndrome are modulated by environment and evolution. Philos Trans R Soc Biol Sci 373:20170428

    Article  Google Scholar 

  • Moran NP, Mossop KD, Thompson RM, Wong BBM (2016) Boldness in extreme environments: temperament divergence in a desert-dwelling fish. Anim Behav 122:125–133

    Article  Google Scholar 

  • Phillips BL, Suarez AV (2012) The role of behavioural variation in the invasion of new areas. In: Wong BBM, Candolin U (eds) Behavioural responses to a changing world: mechansims and consequences. Oxford University Press, Oxford, pp 190–200

    Chapter  Google Scholar 

  • Pilastro A, Benetton S, Bisazza A (2003) Female aggregation and male competition reduce costs of sexual harassment in the mosquitofish Gambusia holbrooki. Anim Behav 65:1161–1167

    Article  Google Scholar 

  • Pintor LM, Sih A, Kerby JL (2009) Behavioral correlations provide a mechanism for explaining high invader densities and increased impacts on native prey. Ecology 90:581–587

    Article  PubMed  Google Scholar 

  • Polverino G, Santostefano F, Díaz-Gil C, Mehner T (2018) Ecological conditions drive pace-of-life syndromes by shaping relationships between life history, physiology and behaviour in two populations of Eastern mosquitofish. Sci Rep 8:14673

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pyke GH (2005) A review of the biology of Gambusia affinis and G. holbrooki. Rev Fish Biol Fisheries 15:339–365

    Article  Google Scholar 

  • Pyke GH (2008) Plague minnow or mosquito fish? A review of the biology and impacts of introduced Gambusia species. Annu Rev Ecol Evol Syst 39:171–191

    Article  Google Scholar 

  • R Core Development Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rebrina F, Skejo J, Lucić A, Hudina S (2015) Triat variability of the signal crayfish (Pacifastacus leniusculus) in a recently invaded region relects potential benefits and trade-offs during dispersal. Aquat Invasions 10:41–50

    Article  Google Scholar 

  • Rehage JS, Sih A (2004) Dispersal behavior, boldness, and the link to invasiveness: a comparison of four Gambusia species. Biol Invasions 6:379–391

    Article  Google Scholar 

  • Rehage JS, Barnett BK, Sih A (2005) Behavioral responses to a novel predator and competitor of invasive mosquitofish and their non-invasive relatives (Gambusia sp.). Behav Ecol Sociobiol 57:256–266

    Article  Google Scholar 

  • Rehage JS, Cote J, Sih A (2016) The role of dispersal behaviour and personality in post-establishment spread. Chapter 7. In: Weis JS, Sol D (eds) Biological invasions and animal behaviour. Cambridge University Press, Cambridge, pp 96–115

    Chapter  Google Scholar 

  • Renault D, Laparie M, McCauley SJ, Bonte D (2018) Environmental adaptations, ecological filtering, and dispersal central to insect invasions. Annu Rev Entomol 63:345–368

    Article  CAS  PubMed  Google Scholar 

  • Royston P (1995) A remark on algorithm AS 181: the W-test for normality. J R Stat Soc Ser C Appl Stat 44:547–551

    Google Scholar 

  • Shaw AK, Kokko H, Neubert MG (2018) Sex difference and Allee effects shape the dynamics of sex-structured invasions. J Anim Ecol 87:36–46

    Article  PubMed  Google Scholar 

  • Shine R (1989) Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Q Rev Biol 64:419–461

    Article  CAS  PubMed  Google Scholar 

  • Shulse CD, Semlitsch RD, Trauth KM (2013) Mosquitofish dominate amphibian and invertebrate community development in experimental wetlands. J Appl Ecol 50:1244–1256

    Article  Google Scholar 

  • Sih A, Bell AM, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378

    Article  PubMed  Google Scholar 

  • Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012) Ecological implications of behavioural syndromes. Ecol Lett 15:278–289

    Article  PubMed  Google Scholar 

  • Tingley R, Romagosa CM, Kraus F, Bickford D, Phillips BL, Shine R (2010) The frog filter: amphibian introduction bias driven by taxonomy, body size and biogeography. Glob Ecol Biogeogr 19:496–503

    Google Scholar 

  • Tomkins P, Saaristo M, Bertram MG, Michelangeli M, Tomkins RB, Wong BBM (2018) An endocrine-disrupting agricultural contaminant impact sequential female mate choice in fish. Environ Pollut 237:103–110

    Article  CAS  PubMed  Google Scholar 

  • Trochet A, Courtois EA, Stevens VM, Baguette M, Chaine A, Schmeller DS, Clobert J, Wiens JJ (2016) Evolution of sex-biased dispersal. Q Rev Biol 91:297–320

    Article  PubMed  Google Scholar 

  • Ward AJ, Thomas P, Hart PJ, Krause J (2004) Correlates of boldness in three-spined sticklebacks (Gasterosteus aculeatus). Behav Ecol Sociobiol 55:561–568

    Article  Google Scholar 

  • Wilson AD, Godin JGJ, Ward AJ (2010) Boldness and reproductive fitness correlates in the eastern mosquitofish, Gambusia holbrooki. Ethology 116:96–104

    Article  Google Scholar 

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Acknowledgements

ARC DP Grant to DGC, AS, and BBMW (DP170100684). Monash University Animal Ethics Approval BSCI/2013/20. JC was supported by a Fyssen Foundation fellowship and an AXA research fund. JC and TB are also supported by a 2012–2013 BiodivERsA COFUND call for research proposals, with the national funders ONEMA, DFG, SEPA. JC works at the Laboratoire Evolution et Diversité Biologique (CNRS, UPS, UMR 5174), part of the Laboratoire d’Excellence (LABEX) entitled TULIP (ANR-10-LABX-41). We would also like to thank three anonymous reviewers for their constructive feedback during the revision process.

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Authors and Affiliations

  1. School of Biological Sciences, Monash University, Melbourne, 3800, Australia

    Marcus Michelangeli, David G. Chapple, Michael G. Bertram, Jack Eades & Bob B. M. Wong

  2. Department of Environmental Science and Policy, University of California, Davis, Davis, CA, 95616, USA

    Marcus Michelangeli, Julien Cote, Andrew Sih, Tomas Brodin & Sean Fogarty

  3. Laboratoire Évolution and Diversité Biologique (EDB UMR 5174), CNRS, IRD, UPS, Université de Toulouse, 118 Route de Narbonne, 31062, Toulouse, France

    Julien Cote

  4. Department of Wildlife, Fish and Environmental Studies, Swedish University of Agricultural Sciences, 901 83, Umeå, Sweden

    Tomas Brodin & Michael G. Bertram

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  1. Marcus Michelangeli
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  2. Julien Cote
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  3. David G. Chapple
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Michelangeli, M., Cote, J., Chapple, D.G. et al. Sex-dependent personality in two invasive species of mosquitofish. Biol Invasions 22, 1353–1364 (2020). https://doi.org/10.1007/s10530-019-02187-3

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