Wing reduction influences male mating success but not female fitness in cockroaches

. 2017 May 24 ; 7 (1) : 2367. [epub] 20170524

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid28539621
Odkazy

PubMed 28539621
PubMed Central PMC5443839
DOI 10.1038/s41598-017-02647-7
PII: 10.1038/s41598-017-02647-7
Knihovny.cz E-zdroje

Although cockroaches (Blattodea s. str.) exhibit high proportion of species with reduced wings, the underlying evolutionary forces remain unclear. Wing reduction in insects is generally considered advantageous for females and a trade-off between investment into the flying apparatus and reproduction is predicted to explain its evolution. However, what if the wing maintenance is an important issue for males' fitness? Males raise wings during the ritualized courtship which is viewed as an unavoidable movement unveiling the tergal glands for female access. We, however, propose a novel male mating success hypothesis suggesting that male wings are essential for their successful mating. We tested these two competing, but not mutually exclusive hypotheses in the cockroach Eublaberus distanti. We found no effect of female wing loss on any of the measured fecundity characteristics despite that alatectomized females histolyzed flight muscles. On the contrary, alatectomized males did not histolyze wing muscles, but experienced a markedly decreased mating success. Our findings, therefore, provide the first evidence on the crucial mechanical role of wings on male mating success. Consequently, selection for the retention of wings in males rather than for their reduction in females can explain the evolution of sexual wing dimorphism in cockroaches and other insects.

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Engel, M. S., Davis, S. R. & Prokop, J. Insect wings: the evolutionary development of nature’s first flyers. In Arthropod Biology and Evolution (ed. Minelli, A., Boxshall, G. & Fusco, G.) 269–298 (Springer Berlin Heidelberg, 2013).

Nicholson DB, Ross AJ, Mayhew PJ. Fossil evidence for key innovations in the evolution of insect diversity. Proceedings of the Royal Society of London B: Biological Sciences. 2014;281:20141823. doi: 10.1098/rspb.2014.1823. PubMed DOI PMC

Roff DA. The evolution of flightlessness in insects. Ecological Monographs. 1990;60:389–421. doi: 10.2307/1943013. DOI

Roff DA. Habitat persistence and the evolution of wing dimorphism in insects. The American Naturalist. 1994;144:772–798. doi: 10.1086/285706. DOI

Wagner DL, Liebherr JK. Flightlessness in insects. Trends in Ecology & Evolution. 1992;7:216–220. doi: 10.1016/0169-5347(92)90047-F. PubMed DOI

Mitterboeck TF, Adamowicz SJ. Flight loss linked to faster molecular evolution in insects. Proceedings of the Royal Society of London B: Biological Sciences. 2013;280:20131128. doi: 10.1098/rspb.2013.1128. PubMed DOI PMC

Ikeda H, Nishikawa M, Sota T. Loss of flight promotes beetle diversification. Nature communications. 2012;3:648. doi: 10.1038/ncomms1659. PubMed DOI PMC

Ikeda H, Kubota K, Kagaya T, Abe T. Flight capabilities and feeding habits of silphine beetles: are flightless species really “carrion beetles”? Ecological research. 2007;22:237–241. doi: 10.1007/s11284-006-0012-1. DOI

Ikeda H, Kagaya T, Kubota K, Abe T. Evolutionary relationships among food habit, loss of flight, and reproductive traits: life‐history evolution in the Silphinae (Coleoptera: Silphidae) Evolution. 2008;62:2065–2079. doi: 10.1111/j.1558-5646.2008.00432.x. PubMed DOI

Fong DW, Kane TC, Culver DC. Vestigialization and loss of nonfunctional characters. Annual Review of Ecology and Systematics. 1995;26:249–268. doi: 10.1146/annurev.es.26.110195.001341. DOI

Lahti DC, et al. Relaxed selection in the wild. Trends in ecology & evolution. 2009;24:487–496. doi: 10.1016/j.tree.2009.03.010. PubMed DOI

Klaus S, et al. Rapid evolution of troglomorphic characters suggests selection rather than neutral mutation as a driver of eye reduction in cave crabs. Biology letters. 2013;9:20121098. doi: 10.1098/rsbl.2012.1098. PubMed DOI PMC

Roff DA. The cost of being able to fly: a study of wing polymorphism in two species of crickets. Oecologia. 1984;63:30–37. doi: 10.1007/BF00379781. PubMed DOI

Lorenz MW. Oogenesis-flight syndrome in crickets: age-dependent egg production, flight performance, and biochemical composition of the flight muscles in adult female Gryllus bimaculatus. Journal of Insect Physiology. 2007;53:819–832. doi: 10.1016/j.jinsphys.2007.03.011. PubMed DOI

Nespolo RF, Roff DA, Fairbairn DJ. Energetic trade-off between maintenance costs and flight capacity in the sand cricket (Gryllus firmus) Functional Ecology. 2008;22:624–631. doi: 10.1111/j.1365-2435.2008.01394.x. DOI

Zera A. J. Differences in survivorship, development rate and fertility between the longwinged and wingless morphs of the waterstrider, Limnoporus canaliculatus. Evolution. 1984;38:1023–1032. doi: 10.2307/2408436. PubMed DOI

Braendle C, Davis GK, Brisson JA, Stern DL. Wing dimorphism in aphids. Heredity. 2006;97:192–199. doi: 10.1038/sj.hdy.6800863. PubMed DOI

Kimura T, Masaki S. Brachypterism and seasonal adaptation in Orgyia thyellina Butler (Lepidoptera, Lymantriidae) Kontyu. 1977;45:97–106.

Gu H, Hughes J, Dorn S. Trade-off between mobility and fitness in Cydia pomonella L. (Lepidoptera: Tortricidae) Ecological Entomology. 2006;31:68–74. doi: 10.1111/j.0307-6946.2006.00761.x. DOI

Jiang XF, Luo LZ, Sappington TW. Relationship of flight and reproduction in beet armyworm, Spodoptera exigua (Lepidoptera: Noctuidae), a migrant lacking the oogenesis-flight syndrome. Journal of Insect Physiology. 2010;56:1631–1637. doi: 10.1016/j.jinsphys.2010.06.006. PubMed DOI

Nishide Y, Tanaka S. The occurence in the migratory locust, Locusta migratoria (Orthoptera: Acrididae), of short-winged morph with. European Journal of Entomology. 2013;110:577–583. doi: 10.14411/eje.2013.078. DOI

Solbreck C, Anderson DB. Wing reduction; its control and consequences in a lygaeid bug, Spilosteth us pandurus. Hereditas. 1989;111:1–6. doi: 10.1111/j.1601-5223.1989.tb00368.x. DOI

Niitepõld K, Boggs CL. Effects of increased flight on the energetics and life history of the butterfly Speyeria mormonia. Plos One. 2015;10:e0140104. doi: 10.1371/journal.pone.0140104. PubMed DOI PMC

Guerra PA. Evaluating the life-history trade-off between dispersal capability and reproduction in wing dimorphic insects: a meta-analysis. Biological Reviews. 2011;86:813–835. doi: 10.1111/j.1469-185X.2010.00172.x. PubMed DOI

Langellotto GA, Denno RF, Ott JR. A trade-off between flight capability and reproduction in males of a wing-dimorphic insect. Ecology. 2000;81:865–875. doi: 10.1890/0012-9658(2000)081[0865:ATOBFC]2.0.CO;2. DOI

Beccaloni, G. W. Cockroach species file online. Version 5.0/5.0. World Wide Web electronic publication. http://Cockroach.SpeciesFile.org [accessed 18 July 2016] (2014).

Chopard, L. La distribution geographique des « Blattinae » apteres ou subapteres (Orth. Blattidae) In Congrès de Liège 975-977 (Association Française pour l’avancement des Sciences) (1924).

Rehn JAG. On apterism and subapterism in the Blattinae (Orthoptera: Blattidae) Entomological News. 1932;43:201–206.

Bell, W. J., Roth, L. M. & Nalepa, C. A. Cockroaches: ecology, behavior, and natural history. (The Johns Hopkins University Press, 2007).

Roth LM. The evolution of male tergal glands in the Blattaria. Annals of The Entomological Society of America. 1969;62:176–208. doi: 10.1093/aesa/62.3.617. DOI

Brossut R, Roth LM. Tergal modifications associated with abdominal glandular cells in the Blattaria. J Morphol. 1977;151:259–298. doi: 10.1002/jmor.1051510206. PubMed DOI

Mondet C, Abed-Veillard D, Gautier P, Farine JP. Could male tergal secretions be consiedered as a nuptial gift in the Madeira cockroach? Animal Behavior. 2008;75:451–460. doi: 10.1016/j.anbehav.2007.04.025. DOI

Schal C, Gautier JY, Bell WJ. Behavioral ecology of cockroaches. Biol. Rev. 1984;59:209–254. doi: 10.1111/j.1469-185X.1984.tb00408.x. DOI

Legendre F, et al. The evolution of social behaviour in Blaberid cockroaches with diverse habitats and social systems: phylogenetic analysis of behavioural sequences. Biological Journal of the Linnean Society. 2014;111:58–77. doi: 10.1111/bij.12199. DOI

Roff DA. Exaptation and the evolution of dealation in insects. Journal of Evolutionary Biology. 1989;2:109–123. doi: 10.1046/j.1420-9101.1989.2020109.x. DOI

Kramer S. Pigmentation in the thoracic musculature of cockroaches and related Orthoptera and the analysis of flight and stridulation. Proceedings of the 10th International Congress of Entomology. 1956;1:569–579.

Farnworth EG. Effects of ambient temperature, humidity, and age on wing-beat frequency of Periplaneta species. Journal of Insect Physiology. 1972;18:827–839. doi: 10.1016/0022-1910(72)90020-0. DOI

Lihoreau M, Rivault C. Tactile stimuli trigger group effects in cockroach aggregations. Anim Behav. 2008;75:1965–1972. doi: 10.1016/j.anbehav.2007.12.006. DOI

Uzsák A, Dieffenderfer J, Bozkurt A, Schal C. Social facilitation of insect reproduction with motor-driven tactile stimuli. Proceedings of the Royal Society of London B: Biological Sciences. 2014;281:20140325. doi: 10.1098/rspb.2014.0325. PubMed DOI PMC

Wendelken PW, Barth RHJ. On the significance of pseudofemale behavior in the neotropical cockroach genera Blaberus, Archimandrita and Byrsotria. Psyche. 1985;92:493–504. doi: 10.1155/1985/97012. DOI

Scharf I, Martin OY. Same-sex sexual behavior in insects and arachnids: prevalence, causes, and consequences. Behav Ecol Sociobiol. 2013;67:1719–1730. doi: 10.1007/s00265-013-1610-x. DOI

Varadínová Z, Stejskal V, Frynta D. Patterns of aggregation behaviour in six species of cockroach: comparing two experimental approaches. Entomologia Experimentalis et Applicata. 2010;136:184–190. doi: 10.1111/j.1570-7458.2010.01016.x. DOI

Wiens JJ. Widespread loss of sexually selected traits: how the peacock lost its spots. Trends in ecology & evolution. 2001;16:517–523. doi: 10.1016/S0169-5347(01)02217-0. DOI

Roff, D. A. The evolution of wing dimorphism in insects. Evolution40, doi:10.2307/2408759 (1986). PubMed

Whiting MF, Bradler S, Maxwell T. Loss and recovery of wings in stick insects. Nature. 2003;421:264–267. doi: 10.1038/nature01313. PubMed DOI

Wahlberg N, Snäll N, Viidalepp J, Ruohomäki K, Tammaru T. The evolution of female flightlessness among Ennominae of the Holarctic forest zone (Lepidoptera, Geometridae) Molecular Phylogenetics and Evolution. 2010;55:929–938. doi: 10.1016/j.ympev.2010.01.025. PubMed DOI

Kooi, C. J. V. d. & Schwander, T. On the fate of sexual traits under asexuality. Biological Reviews89, 805–819, doi:10.1111/brv.12078 (2014). PubMed

Sreng L. Cockroach mating behaviors, sex pheromones and abdominal glands (Dictyoptera:Blaberidae) Journal of Insect Behaviour. 1993;6:715–735. doi: 10.1007/BF01201672. DOI

Gwynne, D. T. Phylogeny of the Ensifera (Orthoptera): a hypothesis supporting multiple origins of acoustical signalling, complex spermatophores and maternal care in crickets, katydids, and weta. Journal of Orthoptera Research, 203–218, doi:10.2307/3503478 (1995).

Grimaldi, D. & Engel, M. S. Evolution of the insects. (Cambridge University Press, 2005).

Padian K, Chiappe LM. The origin and early evolution of birds. Biological Reviews of the Cambridge Philosophical Society. 1998;73:1–42. doi: 10.1017/S0006323197005100. DOI

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