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Sexual differences in age-dependent survival and life span of adults in a natural butterfly population

  • 1.

    Carey, J. R. Insect biodemography. Annu. Rev. Entomol. 46, 79–110 (2001).

    CAS  PubMed  Google Scholar 

  • 2.

    Bronikowski, A. M. & Promislow, D. E. L. Testing evolutionary theories of aging in wild populations. Trends Ecol. Evol. 20, 271–273 (2005).

    PubMed  Google Scholar 

  • 3.

    Stearns, S. C. The evolution of life histories. (Oxford University Press, Oxford, 1992).

  • 4.

    Monaghan, P., Charmantier, A., Nussey, D. H. & Ricklefs, R. E. The evolutionary ecology of senescence. Funct. Ecol. 22, 371–378 (2008).

    Google Scholar 

  • 5.

    Nussey, D. H., Froy, H., Lemaitre, J.-F., Gaillard, J.-M. & Austad, S. N. Senescence in natural populations of animals: Widespread evidence and its implications for bio-gerontology. Ageing Res. Rev. 12, 214–225 (2013).

    PubMed  Google Scholar 

  • 6.

    Vinogradov, A. E. Male reproductive strategy and decreased longevity. Acta Biotheor. 46, 157–160 (1998).

    CAS  PubMed  Google Scholar 

  • 7.

    Bonduriansky, R., Maklakov, A., Zajitschek, F. & Brooks, R. Sexual selection, sexual conflict and the evolution of ageing and life span. Funct. Ecol. 22, 443–453 (2008).

    Google Scholar 

  • 8.

    Nussey, D. H., Coulson, T., Festa-Bianchet, M. & Gaillard, J.-M. Measuring senescence in wild animal populations: towards a longitudinal approach. Funct. Ecol. 22, 393–406 (2008).

    Google Scholar 

  • 9.

    Salguero-Gomez, R. et al. COMADRE: a global data base of animal demography. J. Anim. Ecol. 85, 371–384 (2016).

    PubMed  PubMed Central  Google Scholar 

  • 10.

    Bonduriansky, R. & Brassil, C. E. Rapid and costly ageing in wild male flies. Nature 420, 377 (2002).

    ADS  CAS  PubMed  Google Scholar 

  • 11.

    Kawasaki, N., Brassil, C., Brooks, R. & Bonduriansky, R. Environmental effects on the expression of life span and aging: an extreme contrast between wild and captive cohorts of Telostylinus angusticollis (Diptera: Neriidae). Am. Nat. 172, 346–357 (2008).

    PubMed  Google Scholar 

  • 12.

    Dukas, R. Mortality rates of honey bees in the wild. Insect. Soc. 55, 252–255 (2008).

    Google Scholar 

  • 13.

    Zajitschek, F., Brassil, C. E., Bonduriansky, R. & Brooks, R. Sex effects on life span and senescence in the wild when dates of birth and death are unknown. Ecology 90, 1698–1707 (2009).

    PubMed  Google Scholar 

  • 14.

    Sherratt, T. N. et al. Empirical evidence of senescence in adult damselflies (Odonata: Zygoptera). J. Anim. Ecol. 79, 1034–1044 (2010).

    CAS  PubMed  Google Scholar 

  • 15.

    Rodríguez-Muñoz, R. et al. Comparing individual and population measures of senescence across 10 years in a wild insect population. Evolution 73, 293–302 (2019).

    PubMed  PubMed Central  Google Scholar 

  • 16.

    Rodríguez-Muñoz, R. et al. Slower senescence in a wild insect population in years with a more female-biased sex ratio. Proc. R. Soc. B 286, 2019286 (2019).

    Google Scholar 

  • 17.

    Osváth-Ferencz et al. Population demography of the endangered large blue butterfly Maculinea arion in Europe. J. Insect Conserv. 21, 411–422 (2017).

    Google Scholar 

  • 18.

    Zajitschek, F., Zajitschek, S. & Bonduriansky, R. Senescence in wild insects: Key questions and challenges. Funct. Ecol. 34, 26–37 (2020).

    Google Scholar 

  • 19.

    Boggs, C. L., Watt, W. B. & Ehrlich, P. R. Butterflies: Ecology and Evolution Taking Flight. (University of Chicago Press, Chicago, 2003).

  • 20.

    Haeler, E., Fiedler, K. & Grill, A. What prolongs a butterfly’s life?: trade-offs between dormancy, fecundity and body size. PloS One 9, e111955 (2014).

    ADS  PubMed  PubMed Central  Google Scholar 

  • 21.

    Karl, I. & Fischer, K. Altitudinal and environmental variation in lifespan in the Copper butterfly Lycaena tityrus. Funct. Ecol. 23, 1132–1138 (2009).

    Google Scholar 

  • 22.

    Karlsson, B. & Wiklund, C. Butterfly life history and temperature adaptations; dry open habitats select for increased fecundity and longevity. J. Anim. Ecol. 74, 99–104 (2005).

    Google Scholar 

  • 23.

    Sielezniew et al. Habitat-related differences in the adult longevity of two ecotypes of a specialized butterfly. J. Zool. 307, 93–103 (2019a).

    Google Scholar 

  • 24.

    Gibbs, M. & Van Dyck, H. Butterfly flight activity affects reproductive performance and longevity relative to landscape structure. Oecologia 163, 341–350 (2010).

    ADS  PubMed  Google Scholar 

  • 25.

    Cahenzli, F. & Erhardt, A. Nectar sugars enhance fitness in male Coenonympha pamphilus butterflies by increasing longevity or realized reproduction. Oikos 121, 1417–1423 (2012).

    Google Scholar 

  • 26.

    Molleman, F. et al. Adult diet affects lifespan and reproduction of the fruit-feeding butterfly Charaxes fulvescens. Entomol. Exp. Appl. 129, 54–65 (2008).

    PubMed  PubMed Central  Google Scholar 

  • 27.

    Molleman, F., Ding, J., Boggs, C., Carey, J. R. & Arlet, M. E. Does dietary restriction reduce life span in male fruit-feeding butterflies? Exp. Gerontol. 44, 601–606 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 28.

    Cordero, C. Trade-off between fitness components in males of the polygynous butterfly Callophrys xami (Lycaenidae): the effect of multiple mating on longevity. Behav. Ecol. Sociobiol. 48, 458–462 (2000).

    Google Scholar 

  • 29.

    Kawagoe, T., Suzuki, N. & Matsumoto, K. Multiple mating reduces longevity of females of the windmill butterfly Atrophaneura alcinous. Ecol. Entomol. 26, 258–262 (2001).

    Google Scholar 

  • 30.

    Beck, J. & Fiedler, K. Adult life spans of butterflies (Lepidoptera: Papilionoidea + Hesperioidea): broadscale contingencies with adult and larval traits in multi-species comparisons. Biol. J. Linn. Soc. 96, 166–184 (2009).

    Google Scholar 

  • 31.

    Gotthard, K., Nylin, S. & Wiklund, C. Mating opportunity and the evolution of sex-specific mortality rates in a butterfly. Oecologia 122, 36–43 (2000).

    ADS  CAS  PubMed  Google Scholar 

  • 32.

    Bauerfeind, S. S., Perlick, J. E. C. & Fischer, K. Disentangling environmental effects on adult life span in a butterfly across the metamorphic boundary. Exp. Gerontol. 44, 805–811 (2009).

    PubMed  Google Scholar 

  • 33.

    McCrea, R. S. & Morgan, B. J. T. Analysis of Capture-Recapture Data. (CRC Press, Taylor & Francis Group, Boca Raton, 2014).

  • 34.

    Ehrlich, P. R. & Hanski, I. On the Wings of Checkerspots: A Model System for Population Biology. (Oxford University Press, USA, 2004).

  • 35.

    Settele, J., Shreeve, T., Konvička, M. & Van Dyck, H. Ecology of Butterflies in Europe. (Cambridge University Press, Cambridge, 2009).

  • 36.

    Turlure, C., Pe’er, G., Baguette, M. & Schtickzelle, N. A simplified mark-release-recapture protocol to improve the cost-effectiveness of repeated population size quantification. Methods Ecol. Evol. 9, 645–656 (2018).

    Google Scholar 

  • 37.

    Stevens, V. M., Turlure, C. & Baguette, M. A meta-analysis of dispersal in butterflies. Biol. Rev. 85, 625–642 (2010).

    PubMed  Google Scholar 

  • 38.

    Auckland, J. N., Debinski, D. M. & Clark, W. R. Survival, movement, and resource-use of the butterfly Parnassius clodius. Ecol. Entomol. 29, 139–149 (2004).

    Google Scholar 

  • 39.

    Kőrösi, Á., Örvössy, N., Batáry, P., Harnos, A. & Peregovits, L. Different habitat selection by two sympatric Maculinea butterflies at small spatial scale. Insect Conserv. Diver. 5, 118–126 (2012).

    Google Scholar 

  • 40.

    Nowicki, P. et al. What keeps “living dead” alive: demography of a small and isolated population of Maculinea (=Phengaris) alcon. J. Insect Conserv. 23, 201–210 (2019).

    Google Scholar 

  • 41.

    Skórka, P. et al. Different flight behaviour of the endangered scarce large blue butterfly Phengaris teleius (Lepidoptera: Lycaenidae) within and outside its habitat patches. Landsc. Ecol. 28, 533–546 (2013).

    Google Scholar 

  • 42.

    Schtickzelle, N., Le Boulengé, E. & Baguette, M. Metapopulation dynamics of the bog fritillary butterfly: demographic processes in a patchy population. Oikos 97, 349–360 (2002).

    Google Scholar 

  • 43.

    Zheng, C., Ovaskainen, O., Saastamoinen, M. & Hanski, I. Age‐dependent survival analyzed with Bayesian models of mark–recapture data. Ecology 88, 1970–1976 (2007).

    PubMed  Google Scholar 

  • 44.

    Brakefield, P. M. Ecological studies on the butterfly Maniola jurtina in Britain. II. Population dynamics: the present position. J. Anim. Ecol. 51, 727–738 (1982).

    Google Scholar 

  • 45.

    Bubová, T., Kulma, M., Vrabec, V. & Nowicki, P. Adult longevity and its relationship with conservation status in European butterflies. J. Insect Conserv. 20, 1021–1032 (2016).

    Google Scholar 

  • 46.

    Kahuthia-Gathu, R., Löhr, B. & Poehling, H. M. Development and reproductive potential of diamondback moth Plutella xylostella (Lepidoptera: Plutellidae) on cultivated and wild crucifer species in Kenya. Int. J. Trop. Insect Sci. 28, 19–29 (2008).

    Google Scholar 

  • 47.

    Tolman, T. & Lewington, R. Collins Butterfly Guide. (Harper Collins Publishers, London, 2009).

  • 48.

    Buszko, J. & Masłowski, J. Motyle dzienne Polski. (Wydawnictwo „Koliber”, Nowy Sącz, 2015).

  • 49.

    White, G. C. & Burnham, K. P. Program MARK: Survival estimation from populations of marked animals. Bird Study 46, 120–138 (1999).

    Google Scholar 

  • 50.

    Schwarz, C. J. & Arnason, A. N. A general methodology for the analysis of capture-recapture experiments in open populations. Biometrics 52, 860–873 (1996).

    MathSciNet  MATH  Google Scholar 

  • 51.

    Gaillard, J.-M., Viallefont, A., Loison, A. & Festa-Bianchet, M. Assessing senescence patterns in populations of large mammals. Anim. Biodiv. Conserv. 27, 47–58 (2004).

    Google Scholar 

  • 52.

    Burnham, K. P. & Anderson, D. R. Model selection and multimodel inference: a practical information-theoretic approach. Second Edition. (Springer-Verlag, Berlin, 2002).

  • 53.

    Hurvich, C. M. & Tsai, C. Regression and time series model selection in small samples. Biometrika 76, 297–307 (1989).

    MathSciNet  MATH  Google Scholar 

  • 54.

    Laake, J. L. RMark: an R interface for analysis of capture-recapture data with MARK. Alaska Fisheries Science Center, NOAA, National Marine Fisheries Service, Seattle: AFSC Processed Report 2013-01 (2013).

  • 55.

    R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2016).

  • 56.

    Nowicki, P. et al. Less input same output: simplified approach for population size assessment in Lepidoptera. Popul. Ecol. 47, 203–212 (2005a).

    Google Scholar 

  • 57.

    Parker, G. A. Sexual selection and sexual conflict. In Sexual selection and reproductive competition in insects (ed. Blum, M. S. & Blum, N. A.) 123–166 (Academic Press, New York, 1979).

  • 58.

    Parker, G. A. Sexual conflict over mating and fertilization: an overview. Philos. Trans. R. Soc. B 361, 235–259 (2006).

    CAS  Google Scholar 

  • 59.

    Williams, G. C. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11, 398–411 (1957).

    Google Scholar 

  • 60.

    Hamilton, W. D. The moulding of senescence by natural selection. J. Theor. Biol. 12, 12–45 (1966).

    CAS  PubMed  Google Scholar 

  • 61.

    Kirkwood, T. B. L. & Rose, M. R. Evolution of senescence: late survival sacrificed for reproduction. Philos. Trans. R. Soc. B 332, 15–24 (1991).

    ADS  CAS  Google Scholar 

  • 62.

    Wickman, P.-O. Mating behaviour in butterflies. In Ecology of Butterflies in Europe (ed. Settele, J., Shreeve, T., Konvička, M. & Van Dyck, H.) 17–28 (Cambridge University Press, Cambridge, 2009).

  • 63.

    Wiklund, C. Sexual selection and the evolution of butterfly mating systems. In Butterflies: Ecology and Evolution Taking Flight (ed. Boggs, C. L., Watt, W. B. & Ehrlich, P. R.) 67–90 (University of Chicago Press, Chicago, 2003).

  • 64.

    Rutowski, R. L. Sexual dimorphism, mating systems and ecology in butterflies. In The evolution of mating systems in insects and arachnids (ed. Choe, J. C. & Crespi, B. J.) 257–272 (Cambridge University Press, Cambridge, 1997).

  • 65.

    Kemp, D. J. & Wiklund, C. Fighting without weaponry: a review of male-male contest competition in butterflies. Behav. Ecol. Sociobiol. 49, 429–442 (2001).

    Google Scholar 

  • 66.

    Wiklund, C., Gotthard, K. & Nylin, S. Mating system and the evolution of sex-specific mortality rates in two nymphalid butterflies. Proc. R. Soc. B 270, 1823–1828 (2003).

  • 67.

    Wiklund, C. & Fagerström, T. Why do males emerge before females? Oecologia 31, 153–158 (1977).

    ADS  PubMed  Google Scholar 

  • 68.

    Örvössy, N., Kőrösi, Á., Batáry, P., Vozár, Á. & Peregovits, L. Potential metapopulation structure and the effects of habitat quality on population size of the endangered False Ringlet butterfly. J. Insect Conserv. 17, 537–547 (2013).

    Google Scholar 

  • 69.

    Zimmermann, K., Fric, Z., Filipová, L. & Konvička, M. Adult demography, dispersal and behaviour of Brenthis ino (Lepidoptera: Nymphalidae): how to be a successful wetland butterfly. Eur. J. Entomol. 102, 699–706 (2005).

    Google Scholar 

  • 70.

    Fagerström, T. & Wiklund, C. Why do males emerge before females? Protandry as a mating strategy in male and female butterflies. Oecologia 52, 164–166 (1982).

    ADS  PubMed  Google Scholar 

  • 71.

    Zonneveld, C. Polyandry and protandry in butterflies. Bull. Math. Biol. 54, 957–976 (1992).

    MATH  Google Scholar 

  • 72.

    Doak, P., Kareiva, P. & Kingsolver, J. Fitness consequences of choosy oviposition for a time-limited butterfly. Ecology 87, 395–408 (2006).

    PubMed  Google Scholar 

  • 73.

    Kőrösi, Á., Örvössy, N., Batáry, P., Kövér, S. & Peregovits, L. Restricted within-habitat movement and time-constrained egg laying of female Maculinea rebeli butterflies. Oecologia 156, 455–464 (2008).

    ADS  PubMed  Google Scholar 

  • 74.

    Kemp, D. J., Wiklund, C. & Van Dyck, H. Contest behaviour in the speckled wood butterfly (Pararge aegeria): Seasonal phenotypic plasticity and the functional significance of flight performance. Behav. Ecol. Sociobiol. 59, 403–411 (2006).

    Google Scholar 

  • 75.

    Berwaerts, K. & Van Dyck, H. Take-off performance under optimal and suboptimal thermal conditions in the butterfly Pararge aegeria. Oecologia 141, 536–545 (2004).

    ADS  PubMed  Google Scholar 

  • 76.

    Merckx, T., Karlsson, B. & Van Dyck, H. Sex- and landscape-related differences in flight ability under suboptimal temperatures in a woodland butterfly. Funct. Ecol. 20, 436–441 (2006).

    Google Scholar 

  • 77.

    Boggs, C. L. Understanding insect life histories and senescence through a resource allocation lens. Funct. Ecol. 23, 27–37 (2009).

    Google Scholar 

  • 78.

    Vande Velde, L. & Van Dyck, H. Lipid economy, flight activity and reproductive behaviour in the speckled wood butterfly: on the energetic cost of territory holding. Oikos 122, 555–562 (2013).

    Google Scholar 

  • 79.

    Bergström, J. & Wiklund, C. Effects of size and nuptial gifts on butterfly reproduction: can females compensate for a smaller size through male-derived nutrients? Behav. Ecol. Sociobiol. 52, 296–302 (2002).

    Google Scholar 

  • 80.

    Nowicki, P., Witek, M., Skórka, P., Settele, J. & Woyciechowski, M. Population ecology of the endangered butterflies Maculinea teleius and M. nausithous, and its implications for conservation. Popul. Ecol. 47, 193–202 (2005b).

    Google Scholar 

  • 81.

    Timuș, N., Craioveanu, C., Sitaru, C., Rus, A. & Rákosy, L. Differences in adult phenology, demography, mobility and distribution in two syntopic ecotypes of Maculinea alcon (cruciata vs. pneumonanthe) (Lepidoptera: Lycaenidae) from Transilvania (Romania). Entomol. Romanica. 18, 21–30 (2013).

    Google Scholar 

  • 82.

    Turlure, C., Legrand, D., Schtickzelle, N. & Baguette, M. Male disguised females: costs and benefits of female-limited dimorphism in a butterfly. Ecol. Entomol. 41, 572–581 (2016).

    Google Scholar 

  • 83.

    Beldade, P. & Brakefield, P. M. The genetics and evo-devo of butterfly wing patterns. Nat. Rev. Genet. 3, 442–452 (2002).

    CAS  PubMed  Google Scholar 

  • 84.

    Sielezniew, M., Deoniziak, K., Dziekańska, I. & Nowicki, P. Dispersal in a metapopulation of the critically endangered Danube Clouded Yellow butterfly Colias myrmidone: implications for conservation. J. Insect Conserv. 23, 291–300 (2019).

    Google Scholar 

  • 85.

    Benedick, S. et al. Butterfly dispersal and longevity in unlogged and selectively logged forest. Sepilok Bull. 6, 25–37 (2007).

    Google Scholar 

  • 86.

    Molleman, F., Zwaan, B. J., Brakefield, P. M. & Carey, J. R. Extraordinary long life spans in fruit-feeding butterflies can provide window on evolution of life span and aging. Exp. Gerontol. 42, 472–482 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 


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