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Phylogeographic structure without pre-mating barriers: Do habitat fragmentation and low mobility preserve song and chorus diversity in a European bushcricket?

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Abstract

When animal species have a strong phylogeographic structure questions arise on the origin, maintenance and future evolutionary trajectory of that structure. One prediction is that phenotypic differences among populations serve as pre-mating barriers should secondary contact occur. Post-mating barriers may also function and ensure further separation of the populations. We tested these predictions in an acoustic insect, the European bushcricket Ephippiger diurnus, that is geographically distributed in separated, genetically isolated populations distinguished by pronounced differences in male songs and chorusing and female preferences for song. We staged mixed-population choruses to examine how males sing when in the company of other populations, and we released females in these choruses to assess their preference for or aversion toward males of their own population versus a different one. We also paired males and females of the same and different populations to test mating success, spermatophore transfer, and oviposition in the various pairings. In most cases males sang as effectively when accompanied by males from another population as when in a single-population chorus, and females overall expressed little aversion toward males from a different population. Inter-population pairs did not mate less frequently, transfer smaller spermatophores, or deposit fewer or smaller eggs than pairs of males and females from the same population. We infer that pre-mating barriers play little role in maintaining phylogeographic structure despite the acoustic differences between populations. Rather, the structure probably reflects the fragmented distribution of suitable habitat and the low mobility of both juveniles and adults. Thus, if secondary contact does occur, and we predict that it will in several key locations owing to ongoing environmental change, coalescence of populations and reduction of genetic and acoustic diversity may follow.

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Fig. 1

See Marin-Cudraz and Greenfield (2016) for recording methods and Table 1 for further information on the populations

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References

  • Anderson LW, Fog K, Damgaard C (2004) Habitat fragmentation causes bottlenecks and inbreeding in the European tree frog (Hyla arborea). Proc R Soc Lond B 271:1293–1302

    Article  Google Scholar 

  • Avise JC, Bowen BW, Ayala FJ (2016) In the light of evolution X: comparative phylogeography. Proc Natl Acad Sci 113:7957–7961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barbosa F, Rebar D, Greenfield MD (2016a) Reproduction and immunity trade-offs constrain mating signals and nuptial gift size in a bushcricket. Behav Ecol 27:109–117

    Article  Google Scholar 

  • Barbosa F, Rebar D, Greenfield MD (2016b) Female preference functions drive inter-population divergence in male signaling: call diversity in the bushcricket Ephippiger diurnus. J Evol Biol 29:2219–2228

    Article  CAS  PubMed  Google Scholar 

  • Bateman PW, Ferguson JWH (2004) Male mate choice in the Botswana armoured ground cricket Acanthoplus discoidalis (Orthoptera: Tettigoniidae; Heterodinae). Can, and how, do males judge female mating history? J Zool 262:305–309

    Article  Google Scholar 

  • Bateman PW, Gilson LN, Ferguson JWH (2001) Male size and sequential mate preference in the cricket Gryllus bimaculatus. Anim Behav 61:631–637

    Article  Google Scholar 

  • Bridle JR, Baird SJE, Butlin RK (2001) Spatial structure and habitat variation in a grasshopper hybrid zone. Evolution 55:1832–1843

    Article  CAS  PubMed  Google Scholar 

  • Butlin RK, Hewitt GM (1985) A hybrid zone between Chorthippus parallelus parallelus and Chorthippus parallelus erythropus (Orthoptera, Acrididae)—behavioral characters. Biol J Linn Soc 26:287–299

    Article  Google Scholar 

  • Courchamp F, Clutton-Brock T, Grenfell B (1999) Inverse density dependence and the Allee effect. Trends Ecol Evol 14:405–410

    Article  CAS  PubMed  Google Scholar 

  • Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland

    Google Scholar 

  • Davis BAS, Brewer S, Stevenson AC, Guiot J, Contributors Data (2003) The temperature of Europe during the Holocene reconstructed from pollen data. Quat Sci Rev 22:1701–1716

    Article  Google Scholar 

  • Duijm M (1990) On some song characteristics in Ephippiger (Orthoptera, Tettigonioidea) and their geographic variation. Neth J Zool 40:428–453

    Article  Google Scholar 

  • Esquer-Garrigos Y, Greenfield MD, Party V, Streiff R (2016) Characterization of 16 novel microsatellite loci for Ephippiger diurnus (Orthoptera: Tettigoniidae) using pyrosequencing technology and cross-species amplification. Eur J Entomol 113:302–306

    Article  Google Scholar 

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515

    Article  Google Scholar 

  • Greenfield MD (2005) Mechanisms and evolution of communal sexual displays in arthropods and anurans. Adv Study Behav 35:1–61

    Article  Google Scholar 

  • Greenfield MD (2015) Signal interactions and interference in insect choruses: singing and listening in the social environment. J Comp Physiol A 201:143–154 (Special issue: Insect hearing: From physics to ecology)

    Article  Google Scholar 

  • Greenfield MD (2016) Evolution of acoustic communication in insects. In: Pollack GS, Mason AC (eds) Insect hearing, vol. 5, Springer handbook of auditory research. Springer, Dordrecht, pp 17–47

    Google Scholar 

  • Greenfield MD, Roizen I (1993) Katydid synchronous chorusing is an evolutionarily stable outcome of female choice. Nature 364:618–620

    Article  Google Scholar 

  • Greenfield MD, Snedden WA (2003) Selective attention and the spatio-temporal structure of orthopteran choruses. Behaviour 140:1–26

    Article  Google Scholar 

  • Greenfield MD, Tourtellot MK, Snedden WA (1997) Precedence effects and the evolution of chorusing. Proc R Soc Lond B 264:1355–1361

    Article  Google Scholar 

  • Greenfield MD, Siegfreid E, Snedden WA (2004) Variation and repeatability of female choice in a chorusing katydid, Ephippiger ephippiger: an experimental exploration of the precedence effect. Ethology 110:287–299

    Article  Google Scholar 

  • Greenfield MD, Esquer-Garrigos Y, Streiff R, Party V (2016) Animal choruses emerge from receiver psychology. Sci Rep 6:34369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison RG (1993) Hybrid zones and the evolutionary process. Oxford University Press, Oxford

    Google Scholar 

  • Hartbauer M, Römer H (2016) Rhythm generation and rhythm perception in insects: the evolution of synchronous choruses. Front Neurosci 10:223. doi:10.3389/fnins.2016.00223

    Article  PubMed  PubMed Central  Google Scholar 

  • Hartbauer M, Haitzinger L, Kainz M, Römer H (2014) Competition and cooperation in a synchronous bushcricket chorus. R Soc Open Sci 1(2):140167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276

    Article  Google Scholar 

  • Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112

    Article  Google Scholar 

  • Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913

    Article  CAS  PubMed  Google Scholar 

  • Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philos Trans R Soc Lond B 359:183–195

    Article  CAS  Google Scholar 

  • Hockham LR, Graves JA, Ritchie MG (2001) Variable maternal control of facultative egg diapause in the bushcricket Ephippiger ephippiger. Ecol Entomol 26:143–147

    Article  Google Scholar 

  • Jarrige A, Greenfield MD, Goubault M (2013) Male song as a predictor of the nuptial gift in bushcrickets on the confounding influence of male choice. Anim Behav 85:1427–1434

    Article  Google Scholar 

  • Kidd DM, Ritchie MG (2000) Inferring the patterns and causes of geographic variation in Ephippiger ephippiger (Orthoptera, Tettigoniidae) using geographical information systems (GIS). Biol J Linn Soc 71:269–295

    Article  Google Scholar 

  • Larson EL, Becker CG, Bondra ER, Harrison RG (2013) Structure of a mosaic hybrid zone between the field crickets Gryllus firmus and G. pennsylvanicus. Ecol Evol 3:985–1002

    Article  PubMed  PubMed Central  Google Scholar 

  • Liou LW, Price TD (1994) Speciation by reinforcement of premating isolation. Evolution 48:1451–1459

    Article  PubMed  Google Scholar 

  • Lovette IJ (2005) Glacial cycles and the tempo of avian speciation. Trends Ecol Evol 20:57–59

    Article  PubMed  Google Scholar 

  • Marin-Cudraz T, Greenfield MD (2016) Finely tuned choruses: bushcrickets adjust attention to neighboring singers in relation to the acoustic environment they create. Behav Ecol Sociobiol 70:1581–1589

    Article  Google Scholar 

  • Minckley RL, Greenfield MD, Tourtellot MK (1995) Chorus structure in tarbush grasshoppers: inhibition, selective phonoresponse, and signal competition. Anim Behav 50:579–594

    Article  Google Scholar 

  • Muller KL (1998) The role of conspecifics in habitat settlement in a territorial grasshopper. Anim Behav 56:479–486

    Article  CAS  PubMed  Google Scholar 

  • Muller KL, Stamps JA, Krishnan VV, Willits NH (1997) The effects of conspecificattraction and habitat quality on habitat selection in territorial birds (Troglodytes aedon). Am Nat 150:650–661

    Article  CAS  PubMed  Google Scholar 

  • Nosil P (2012) Ecological speciation. Oxford University Press, Oxford

    Book  Google Scholar 

  • Ortiz-Barrientos D, Counterman BA, Noor MAF (2004) The genetics of speciation by reinforcement. PLoS Biol 2:2256–2263

    Article  CAS  Google Scholar 

  • Party V, Brunel-Pons O, Greenfield MD (2014) Priority of precedence: receiver psychology, female preference for leading calls and sexual selection in insect choruses. Anim Behav 87:175–185

    Article  Google Scholar 

  • Party V, Streiff R, Marin-Cudraz T, Greenfield MD (2015) Group synchrony and alternation as an emergent property: elaborate chorus structure in a bushcricket is an incidental byproduct of female preference for leading calls. Behav Ecol Sociobiol 69:1957–1973

    Article  Google Scholar 

  • Rebar D, Barbosa F, Greenfield MD (2016) Acoustic experience influences male and female pre- and postcopulatory behaviors in a bushcricket. Behav Ecol 27:434–443

    Article  Google Scholar 

  • Ritchie MG (1991) Female preference for ‘song races’ of Ephippiger ephippiger (Orthoptera: Tettigoniidae). Anim Behav 42:518–520

    Article  Google Scholar 

  • Ritchie MG (1992) Variation in male song and female preference within a population of Ephippiger ephippiger (Orthoptera: Tettigoniidae). Anim Behav 43:845–855

    Article  Google Scholar 

  • Ritchie MG (1996) The shape of female mating preferences. Proc Natl Acad Sci 93:14628–14631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ritchie MG, Kidd DM, Gleason JM (2001) Mitochondrial DNA variation and GIS analysis confirm a secondary origin of geographical variation in the bushcricket Ephippiger ephippiger (Orthoptera: Tettigonioidea), and resurrect two subspecies. Mol Ecol 10:603–611

    Article  CAS  PubMed  Google Scholar 

  • Schwander T, Arbuthnott D, Gries R, Gries G, Nosil P, Crespi BJ (2013) Hydrocarbon divergence and reproductive isolation in Timema stick insects. BMC Evol Biol 13:151. doi:10.1186/1471-2148-13-151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Servedio MR, Van Doorn GS, Kopp M, Frame AM, Nosil P (2011) Magic traits in speciation: ‘Magic’ but not rare? Trends Ecol Evol 26:389–397

    Article  PubMed  Google Scholar 

  • Shapiro LH (2001) Asymmetric assortative mating between two hybridizing Orchelimum katydids (Orthoptera: Tettigoniidae). Am Midl Nat 145:423–427

    Article  Google Scholar 

  • Snedden WA, Greenfield MD, Jang Y (1998) Mechanisms of selective attention in grasshopper choruses: who listens to whom? Behav Ecol Sociobiol 43:59–66

    Article  Google Scholar 

  • Spooner LJ, Ritchie MG (2006) An unusual phylogeography in the bushcricket Ephippiger ephippiger from southern France. Heredity 97:398–408

    Article  CAS  PubMed  Google Scholar 

  • Stephens PA, Sutherland WJ, Freckleton RP (1999) What is the Allee effect? Oikos 87:185–190

    Article  Google Scholar 

  • Taberlet P, Fumagalli L, Wust-Saucy A-G, Cosson J-F (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464

    Article  CAS  PubMed  Google Scholar 

  • Taylor CM, Hastings A (2005) Allee effects in biological invasions. Ecol Lett 8:895–908

    Article  Google Scholar 

  • Terral J-F, Mengual X (1999) Reconstruction of Holocene climate in southern France and eastern Spain using quantitative anatomy of olive wood and archaeological charcoal. Palaeogeogr Palaeoclimatol Palaeoecol 153:71–92

    Article  Google Scholar 

  • Weiss S, Ferrand N (2007) Phylogeography of southern European refugia: evolutionary perspectives on the origins and conservation of European biodiversity. Springer, Dordrecht

    Book  Google Scholar 

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Acknowledgements

We thank Flavia Barbosa, Guy Bourdais, Marine Deluen, Séverine Devers, Caroline Hébert for technical assistance in the laboratory, Guillaume Baudouin for helping to prepare the maps shown in Fig. 2a, Christophe Bressac and Claude Chevrier for making laboratory space available, Jean-Paul Monge for his special interest in the project, and the Agence Nationale de la Recherche de France (contrat ANR-11-BSV7-025-01; EVOLCHOR), the Centre National de la Recherche Scientifique (CNRS), and the Université François Rabelais de Tours for their financial support. Flavia Barbosa, Raphael Boulay, Yareli Esquer-Garrigos, Darren Rebar, Réjane Streiff, Matthew Symonds and several anonymous referees provided valuable criticisms of earlier versions of this manuscript.

Funding

This study was funded by Grant ANR-11-BSV7-025-01 from the Agence Nationale de la Recherche de France.

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  1. Mathieu Mahamoud-Issa

    Present address: Department of Behavioural Ecology, Institute of Environmental Sciences, Faculty of Biology, Adam Mickiewicz University, Poznan, Poland

  2. Thibaut Marin-Cudraz

    Present address: Equipe Neuro-Ethologie Sensorielle, ENES/Neuro-PSI, CNRS, UMR 9197, Université de Lyon/Saint-Etienne, 42023, Saint Etienne, France

Authors and Affiliations

  1. CNRS, UMR 7261, Parc de Grandmont, Institut de recherche sur la biologie de l’insecte, Université François Rabelais de Tours, 37200, Tours, France

    Mathieu Mahamoud-Issa, Thibaut Marin-Cudraz, Virginie Party & Michael D. Greenfield

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  1. Mathieu Mahamoud-Issa
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Correspondence to Michael D. Greenfield.

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Mahamoud-Issa, M., Marin-Cudraz, T., Party, V. et al. Phylogeographic structure without pre-mating barriers: Do habitat fragmentation and low mobility preserve song and chorus diversity in a European bushcricket?. Evol Ecol 31, 865–884 (2017). https://doi.org/10.1007/s10682-017-9914-3

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