Abstract
Speciation is nowadays recognized as a dynamic process in which the respective roles of forces driving ecological differentiation and reproductive isolation can change through time and space. Incipient speciation events are particularly useful to follow such processes that are not tractable when considering well-differentiated taxa. A promising case study was discovered in the pine processionary moth, Thaumetopoea pityocampa, a Mediterranean defoliator of Pinus species, for which allochrony acting as an automatic magic trait was recognized as the major driver of an incipient speciation process. In Portugal, a unique population with a shifted phenology, known as the summer population (SP), co-occurs with a population following the typical life cycle, known as the winter population (WP). We monitored male activity of both populations in the Leiria region, i.e. over the whole SP distribution range using a systematic sampling along two transects, and studied Portuguese WPs at a larger geographical scale to explore their genetic diversity and spatial pattern of differentiation. Results showed that the WPs were genetically more diverse than the SP, with a strong pattern of isolation by distance both at large and small spatial scales, while the SP was very homogeneous over its whole range, without signature of its recent spatial expansion. Contrary to our expectations, no F1 hybrids were identified, even though we found an extended flight period of the SP, overlapping with the beginning of the WP reproductive period. Interestingly, the SP was found to be mostly limited to the sea shore where the WP is now scarce or absent, which could suggest competitive exclusion. Once clearly occurring in a sympatric context, the allochronic differentiation tends to develop nowadays in parapatry.
Similar content being viewed by others
References
A’Hara SW, Amouroux P, Argo EE et al (2012) Permanent genetic resources added to molecular ecology resources database 1 August 2011–30 September 2011. Mol Ecol Resour 12:185–189
Aguilée R, Lambert A, Claessen D (2011) Ecological speciation in dynamic landscapes. J Evol Biol 24:2663–2677
Anderson C, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229
Baack E (2004) Cytotype segregation on regional and microgeographic scales in snow buttercups (Ranunculus adoneus: Ranunculaceae). Am J Bot 91(11):1783–1788
Battisti A (1988) Host-plant relationships and population dynamics of the pine processionary caterpillar Thaumetopoea pityocampa (Denis and Schiffermüller). J Appl Entomol 105:393–402
Battisti A, Avci M, Avtzis DN et al (2015) Natural history of the processionary moths (Thaumetopoea spp.): new insights in relation to climate change. In: Roques A (ed) Processionary moths and climate change: an update. Springer, Dordrecht, pp 15–80
Bolnik DI, Fitzpatrick BM (2007) Sympatric speciation: models and empirical evidence. Annu Rev Ecol Evol Syst 38:459–487
Bosc A (1999) Etude expérimentale du fonctionnement hydrique et carboné des organes aériens du Pin maritime (Pinus pinaster Ait.). Ph.D. Thesis, Université de Bordeaux 2, Bordeaux, France
Branco M, Paiva M-R, Santos H, Burban C, Kerdelhué C (2017) Experimental evidence for heritable reproductive time in 2 allochronic populations of pine processionary moth. Insect Sci 24:325–335
Bull CM (1991) Ecology of parapatric distributions. Annu Rev Ecol Syst 22:19–36
Burban C, Gautier M, Leblois R, Landes J, Santos H, Paiva M-R, Branco M, Kerdelhué C (2016) Evidence for low-level hybridization between two allochronic populations of the pine processionary moth, Thaumetopoea pityocampa (Lepidoptera: Notodontidae). Biol J Linn Soc 199:311–328
Burton TL, Husband BC (2000) Fitness differences among diploids, tetraploids and their triploid progeny in Chamerion angiistifolium (Onagraceae): mechanisms of inviability and implication for polyploid evolution. Evolution 54(4):1182–1191
Butlin R, Galindo J, Grahame JW (2008) Sympatric, parapatric or allopatric: the most important way to classify speciation? Philos Trans R Soc B Biol Sci 363:2997–3007
Canestrelli D, Porreta D, Lowe WH, Bisconti R, Carere C, Nascetti G (2016) The tangled evolutionary legacies of range expansion and hybridization. Trends Ecol Evol 31(9):677–688
Case TJ, Holt RD, McPeek MA, Keitt TH (2005) The community context of species’ borders: ecological and evolutionary perspectives. Oikos 108:28–40
Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24(3):621–631
Démolin G (1969) Comportement des adultes de Thaumetopoea pityocampa Schiff. Dispersion spatiale, importance écologique. Ann Sci For 26(1):81–102
Denno RF, McClure MS, Ott JR (1995) Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annu Rev Entomol 40:297–331
Dieckman U, Doebeli M, Metz JAJ, Tautz D (eds) (2004) Adaptive speciation. Cambridge University Press, Cambridge
Durrett R, Buttel L, Harrison R (2000) Spatial models for hybrid zones. Heredity 84:9–19
Earl DA, von Holdt BM (2012) Structure harvester: a website and program for visualizing structure output and implementing the Evanno method. Conserv Genet Resour 4:359–361
Endler JA (1977) Geographic variation, speciation, and clines. Princeton University Press, Princeton
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620
Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinf Online 1:47–50
Fisher-Reid MC, Engstrom TN, Kuczinsky CA, Stephens PR, Wiens JJ (2013) Parapatric divergence of sympatric morphs in a salamander: incipient speciation on Long Island? Mol Ecol 22:4681–4694
Gavrilets S, Li H, Vose MD (2000) Patterns of parapatric speciation. Evolution 54(4):1126–1134
Glaubitz JC (2004) CONVERT: A user-friendly program to reformat diploid genotypic data for commonly used population genetic software packages. Mol Ecol Notes 4:309–310
Godefroid M, Rocha S, Santos H, Paiva M-R, Burban C, Kerdelhué C, Branco M, Rasplus J-Y, Rossi J-P (2016) Climate constrains range expansion of an allochronic population of the pine processionary moth. Divers Distrib 22(12):1288–1300
Gompert Z, Buerkle CA (2010) Introgress: a software package for mapping components of isolation in hybrids. Mol Ecol Resour 10:378–384
Gröning J, Hochkirch A (2008) Reproductive interference between animal species. Q Rev Biol 33(3):257–282
Harrison RG (1990) Hybrid zones: windows on evolutionary process. Oxford Surv Evol Biol 7:69–128
Hewitt GM (1989) The subdivision of species by hybrid zones. In: Otte D, Endler JA (eds) Speciation and its consequences. Sinauer, Sunderland, pp 85–110
Hewitt GM (2011) Quaternary phylogeography: the roots of hybrid zones. Genetica 139:617–638
Hodar JA, Torres-Muros L, Zamora R, Antonio J, Perez-Luque AJ, Senhadji K (2015) No evidence of induced defense after defoliation in three pine species against an expanding pest, the pine processionary moth. For Ecol Manag 356:166–172
Hoskin CJ, Higgie M (2010) Speciation via species interactions: the divergence of mating traits within species. Ecol Lett 13(4):409–420
Ingram T (2011) Speciation along a depth gradient in a marine adaptive radiation. Proc R Soc Lond B 278:613–618
Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405
Kerdelhué C, Magnoux E, Lieutier F, Roques A, Rousselet J (2006) Comparative population genetic study of two oligophagous insects associated with the same hosts. Heredity 97(1):38–45
Kerdelhué C, Zane L, Simonato M, Salvato P, Rousselet J, Roques A, Battisti A (2009) Quaternary history and contemporary patterns in a currently expanding species. BMC Evol Biol 9:220
Kerdelhué C, Battisti A, Burban C et al (2015) Genetic diversity and structure at different spatial scales in the processionary moths. In: Roques A (ed) Processionary moths and climate change: an update. Springer, Dordrecht, pp 163–226
Kisel Y, Barraclough TG (2010) Speciation has a spatial scale that depends on levels of gene flow. Am Nat 175(3):316–334
Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: A program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15(5):1179–1191
Leblois R, Rousset F, Estoup A (2004) Influence of spatial and temporal heterogeneities of the estimation of demographic parameters in a continuous population using individual microsatellite data. Genetics 166:1081–1092
Leblois R, Gautier M, Rohfritsch A, Foucaud J, Burban C, Galan M, Loiseau A, Sauné L, Branco M, Gharbi K, Vitalis R, Kerdelhué C (2018) Deciphering the demographic history of allochronic differentiation in the pine processionary moth Thaumetopoea pityocampa. Mol Ecol 27:264–278
Lombardero MJ, Ayres MP, Bonello P, Cipollini D, Herms DA (2016) Effects of defoliation and site quality on growth and defenses of Pinus pinaster and P. radiate. Forest Ecol Manag 382:39–50
Matute DR, Coyne JA (2010) Intrinsic reproductive isolation between two sister species of Drosophila. Evolution 64(4):903–920
Mayr E (1942) Systematics and the origin of species. Columbia University Press, New York
Mayr E (1963) Animal Species and Evolution. Belknap Press, Cambridge
Miller RS (1967) Pattern and process in competition. Adv Ecol Res 4:1–74
Nielsen EE, Bach L, Kotlicki P (2006) HYBRIDLAB (version 1.0): a program for generating simulated hybrids from population samples. Mol Ecol Notes 6:971–973
Nosil P (2012) Ecological speciation. Oxford series in ecology and evolution. Oxford University Press, Oxford
Nykänen H, Koricheva J (2004) Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis. Oikos 104:247–268
Paiva M-R, Mateus E, Santos MH, Branco MR (2011) Pine volatiles mediate host selection for oviposition by Thaumetopoea pityocampa (Lep., Notodontidae). J Appl Ent 135:195–203
Pettengill JB, Moeller DA (2012) Phylogeography of speciation: allopatric divergence and secondary contact between outcrossing and selfing Clarkia. Mol Ecol 21(18):4578–4592
Pimentel C, Calvão T, Santos M, Ferreira C, Neves M, Nilsson JA (2006) Establishment and expansion of a Thaumetopoea pityocampa (Den. and Schiff.) (Lep. Notodontidae) population with a shifted life cycle in a production pine forest, Central-Coastal Portugal. For Ecol Manag 233:108–115
Pimentel CS, Ferreira C, Santos M, Calvão T (2017) Spatial patterns at host and forest stand scale and population regulation of the pine processionary moth Thaumetopoea pityocampa. Agric For Entomol 19:200–209
Pritchard JK, Stephens M, Donnely P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Robinet C, Laparie M, Rousselet J (2015) Looking beyond the large scale effects of global change: local phenologies can result in critical heterogeneity in the pine processionary moth. Front Physiol 6:334
Roitto M, Rautio P, Markkola A, Julkunen-Tiitto R, Varama M, Saravesi K, Tuomi J (2009) Induced accumulation of phenolics and sawfly performance in Scots pine in response to previous defoliation. Tree Physiol 29:207–216
Roques A, Rousselet J, Avci M et al (2015) Climate warming and past and present distribution of the processionary moths (Thaumetopoea spp.) in Europe, Asia Minor and North Africa. In: Roques A (ed) Processionary moths and climate change: an update. Springer, Dordrecht, pp 81–161
Rossi J-P, Garcia J, Roques A, Rousselet J (2016) Trees outside forest in agricultural landscapes: spatial distribution and impact on habitat connectivity for forest organisms. Landsc Ecol 31:243–254
Rousselet J, Magnoux E, Kerdelhué C (2004) Characterization of five microsatellite loci in the pine processionary moth Thaumetopoea pityocampa (Lepidoptera Notodontidae Thaumetopoeinae). Mol Ecol Notes 4:213–214
Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145(4):1219–1228
Rousset F (2000) Genetic differentiation between individuals. J Evol Biol 13:58–62
Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106
Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8:336–352
Salvato P, Simonato M, Zan L, Patarnello T, Masutti L, Battisti A (2005) Do sexual pheromone traps provide biased information of the local gene pool in the pine processionary moth? Agric For Entomol 7(2):127–132
Samalens J-C, Rossi J-P (2011) Does landscape composition alter the spatiotemporal distribution of the pine processionary moth in a pine plantation forest? Popul Ecol 53:287–296
Santos H, Rousselet J, Magnoux E, Paiva M-R, Branco M, Kerdelhué C (2007) Genetic isolation through time: allochronic differentiation of a phenologically atypical population of the pine processionary moth. Proc R Soc Lond B 274:935–941
Santos H, Burban C, Rousselet J, Rossi J-P, Branco M, Kerdelhué C (2011a) Incipient allochronic speciation in the pine processionary moth Thaumetopoea pityocampa (Lepidoptera, Notodontidae). J Evol Biol 24:146–158
Santos H, Paiva M-R, Tavares C, Kerdelhué C, Branco M (2011b) Temperature niche shift observed in a Lepidoptera population under allochronic divergence. J Evol Biol 24:1897–1905
Santos HM, Paiva M-R, Rocha S, Kerdelhué C, Branco M (2013) Phenotypic divergence in reproductive traits of a moth population experiencing a phenological shift. Ecol Evol 3(15):5098–5108
Sauné L, Abella F, Kerdelhué C (2015) Isolation, characterization and PCR multiplexing of 17 microsatellite loci in the pine processionary moth Thaumetopoea pityocampa (Lepidoptera, Notodontidae). Conserv Genet Resour 7:755–757
Seehausen O, Terai Y, Magalhaes IS et al (2008) Speciation through sensory drive in cichlid fish. Nature 455(2):620–626
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
Stuessy TF, Weiss-Schneeweiss H, Keil D (2004) Diploid and polyploid cytotype distribution in Melampodium cinereum and M. leucanthum (Asteraceae, Heliantheae). Am J Bot 91(6):889–898
Tamburini G, Marini L, Hellrigl K, Salvadori C, Battisti A (2013) Effects of climate and density-dependent factors on population dynamics of the pine processionary moth in the Southern Alps. Clim Change 121:701–712
Taylor RS, Friesen VL (2017) The role of allochrony in speciation. Mol Ecol 26:3330–3342
Thibert-Plante X, Gavrilets S (2013) Evolution of mate choice and the so-called magic traits in ecological speciation. Ecol Lett 16:1004–1013
Vähä J-P, Primmer CR (2006) Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol Ecol 15:63–72
Weinstein BG, Graham CH, Parra J (2017) The role of environment, dispersal and competition in explaining reduced co-occurrence among related species. PLoS ONE 12(11):e0185493
Weiss-Schneeweiss H, Emadzade K, Jang T-S, Schneeweiss GM (2013) Evolutionary consequences, constraints and potential of polyploidy in Plants. Cytogenet Genome Res 140:137–150
Wright S (1943) Isolation by distance. Genetics 28:114–138
Acknowledgements
We thank Liliana Vilas Boas for her help with fieldwork and Helena Santos for technical advice during DNA extractions. We are grateful to Flora Abella who participated in DNA extractions. We acknowledge J. Rousselet (URZF, INRA Orléans, France) for providing the larvae from Varges. We are grateful to two anonymous reviewers for their helpful suggestions. Data used in this work were partly produced through the GenSeq molecular genetic analysis technical facilities of the Labex CeMEB, and ANR “Investissements d’Avenir” program (ANR-10-LABX-04-01). This study was partly financed by Fundação para a Ciência e Tecnologia, FCT-MCES, Portugal, (Project Pest-OE/AGR/UI0239/2011) and the Agence Nationale de la Recherche, France (Project GENO-SPACE ANR-16-CE02-0008). It was also supported by Susana Rocha Ph.D. scholarship with the reference SFRH/BD/90188/2012(FCT-MCES).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Burban, C., Rocha, S., Leblois, R. et al. From sympatry to parapatry: a rapid change in the spatial context of incipient allochronic speciation. Evol Ecol 34, 101–121 (2020). https://doi.org/10.1007/s10682-019-10021-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10682-019-10021-4