Mechanisms leading to sympatric speciation are diverse and may build up reproductive isolation. Reproductive isolation among differentiated clades may exist due to genetic incompatibilities, sexual selection, differences in parity mode, reduced post-zygotic survival or reproductive success of hybrids. Here, we test whether differences in parity mode lead to reproductive isolation by investigating introgression in Zootoca vivipara, a lizard species exhibiting oviparous and viviparous reproduction. We measured introgression in transects spanning different viviparous clades, different oviparous subclades, transects containing oviparous and viviparous clades, and transects within the same subclade (control transects). Introgression in transects spanning oviparous and viviparous clades was one order of magnitude smaller than transects spanning the same reproductive mode and no statistical differences existed between transects spanning the same reproductive mode and control transects. Among types of transects, no significant differences existed in genetic and geographic distances, nor number of detected alleles. Moreover, hybrids were detected in all types of transects, showing that parity mode alone does not necessarily lead to complete reproductive isolation, which suggests that reinforcement may play an important role. The evolution of different parity modes together with reinforcement may thus promote reproductive isolation and rapid speciation, potentially explaining why only six of the almost 40,000 vertebrates belonging to groups consisting of viviparous and oviparous species exhibit bimodal reproduction.
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Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.qp7539t.
Allendorf FW, Luikart G, Aitken SN (2012) Conservation and the genetics of populations. Wiley-Blackwell, Sussex, UK
Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229
Arrayago MJ, Bea A, Heulin B (1996) Hybridization experiment between oviparous and viviparous strains of Lacerta vivipara: a new insight into the evolution of viviparity in reptiles. Herpetologica 52:333–342
Blackburn DG (1999) Are viviparity and egg-guarding evolutionarily labile in squamates? Herpetologica 55:556–573
Boughman JW (2001) Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411:944–948. https://doi.org/10.1038/35082064
Braz HB, Scartozzoni RR, Almeida-Santos SM (2016) Reproductive modes of the South American water snakes: a study system for the evolution of viviparity in squamate reptiles. Zool Anz 263:33–44. https://doi.org/10.1016/j.jcz.2016.04.003
Breedveld MC, Fitze PS (2015) A matter of time: delayed mate encounter postpones mating window initiation and reduces the strength of female choosiness. Behav Ecol Sociobiol 69:533–541. https://doi.org/10.1007/s00265-014-1864-y
Breedveld MC, Fitze PS (2016) The timing and interval of mate encounter affects investment during mating. BiolJ Linn Soc 118:610–617. https://doi.org/10.1111/bij.12747
Breedveld MC, San Jose LM, Romero-Diaz C, Roldan ERS, Fitze PS (2017) Mate availability affects the trade-off between producing one or multiple annual clutches. Anim Behav 123:43–51. https://doi.org/10.1016/j.anbehav.2016.10.025
Cornetti L, Belluardo F, Ghielmi S, Giovine G, Ficetola GF, Bertorelle G et al. (2015a) Reproductive isolation between oviparous and viviparous lineages of the Eurasian common lizard Zootoca vivipara in a contact zone. Biol J Linn Soc 114:566–573. https://doi.org/10.1111/bij.12478
Cornetti L, Ficetola GF, Hoban S, Vernesi C (2015b) Genetic and ecological data reveal species boundaries between viviparous and oviparous lizard lineages. Heredity 115:517–526. https://doi.org/10.1038/hdy.2015.54
Cornetti L, Griffith OW, Benazzo A, Panziera A, Whittington CM, Thompson MB et al. (2017) Candidate genes involved in the evolution of viviparity: a RAD sequencing experiment in the lizard Zootoca vivipara (Squamata: Lacertidae). Zool J Linn Soc 183:196–207. https://doi.org/10.1093/zoolinnean/zlx069
Faria R, Navarro A (2010) Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends Ecol Evol 25:660–669. https://doi.org/10.1016/j.tree.2010.07.008
Fitze PS, Cote J, Clobert J (2010) Mating order-dependent female mate choice in the polygynandrous common lizard Lacerta vivipara. Oecologia 162:331–341. https://doi.org/10.1007/s00442-009-1463-1
Fitze PS, Cote J, Martínez-Rica JP, Clobert J (2008) Determinants of male fitness: disentangling intra- and inter-sexual selection. J Evol Biol 21:246–255. https://doi.org/10.1111/j.1420-9101.2007.01447.x
Fitze PS, Le Galiard J-F, Federici P, Richard M, Clobert J (2005) Conflict over multiple-partner mating between males and females of the polygynandrous common lizards. Evolution 59:2451–2459. https://doi.org/10.1554/05-208.1
Fitze PS, Le Galliard JF (2008) Operational sex ratio, sexual conflict and the intensity of sexual selection. Ecol Lett 11:432–439. https://doi.org/10.1111/j.1461-0248.2008.01158.x
Griffith OW, Blackburn DG, Brandley MC, Van Dyke JU, Whittington CM, Thompson MB (2015) Ancestral state reconstructions require biological evidence to test evolutionary hypotheses: a case study examining the evolution of reproductive mode in Squamate reptiles. J Exp Zool B: Mol Dev Evol 324:493–503. https://doi.org/10.1002/jez.b.22614
Hardy OJ, Vekemans X (1999) Isolation by distance in a continuous population: reconciliation between spatial autocorrelation analysis and population genetics models. Heredity 83:145–154. https://doi.org/10.1046/j.1365-2540.1999.00558.x
Harrison RG (1993) Hybrid zones and the evolutionary process. Oxford University Press, Ithaca, New York, NY
Horreo JL, Machado-Schiaffino G, Griffiths AM, Bright D, Stevens JR, Garcia-Vazquez E (2014) Long-term effects of stock transfers: synergistic introgression of allochthonous genomes in salmonids. J Fish Biol 85:292–306. https://doi.org/10.1111/jfb.12424
Horreo JL, Peláez ML, Breedveld MB, Suárez T, Urieta M, Fitze PS (2019) Population structure of the oviparous South-West European common lizard. Eur J Wild Res 65:11. https://doi.org/10.1007/s10344-018-1242-6
Horreo JL, Peláez ML, Fitze PS (2015) Skin sheds as a useful DNA source for lizard conservation. Phyllomedusa 14:73–77. https://doi.org/10.11606/issn.2316-9079.v14i1p73-77
Horreo JL, Peláez ML, Suárez T, Breedvled MC, Heulin B, Surget-Groba Y et al. (2018) Phylogeography, evolutionary history, and effects of glaciations in a species (Zootoca vivipara) inhabiting multiple biogeographic regions. J Biogeogr 45:1616–1627. https://doi.org/10.1111/jbi.13349
Horreo JL, Peláez ML, Suárez T, Heulin B, Fitze PS (2017) Development of thirty-four new microsatellite loci and multiplexing of seven existing loci for Zootoca vivipara. Phyllomedusa 16:89–96. https://doi.org/10.11606/issn.2316-9079.v16i1p89-96
IUCN - International Union for Conservation of Nature (2018) IUCN Red List of threatened species. Version 2018, IUCN, Gland, Switzerland.
Jamieson BGM (2009) Reproductive biology and phylogeny of fishes (agnathans and bony fishes). Science Publishers, Enfield, NH
Kupriyanova L, Kuksin A, Odierna G (2008) Karyotype, chromosome structure, reproductive modalities of three Southern Eurasian populations of the common lacertid lizard, Zootoca vivipara (Jacquin, 1787). Acta Herpetol 3:99–106. https://doi.org/10.13128/Acta_Herpetol-2677
Kvist L, Martens J, Higuchi H, Nazarenko AA, Valchuk OP, O’rell M (2002) Evolution and genetic structure of the great tit (Parus major) complex. Proc R Soc B 270:1447–1454. https://doi.org/10.1098/rspb.2002.2321
Lindtke D, Mayer W, Böhme W (2010) Identification of a contact zone between oviparous and viviparous common lizards (Zootoca vivipara) in central Europe: reproductive strategies and natural hybridization. Salamandra 46:73–82
Matschiner M, Salzburger W (2009) TANDEM: integrating automated allele binning into genetics and genomics workflows. Bioinformatics 25:1982–1983. https://doi.org/10.1093/bioinformatics/btp303
Merimans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794. https://doi.org/10.1111/j.1471-8286.2004.00770.x
Mila B, Surget-Groba Y, Heulin B, Gosá A, Fitze PS (2013) Multilocus phylogeography of the common lizard Zootoca vivipara at the Ibero-Pyrenean suture zone reveals lowland barriers and high-elevation introgression. BMC Evol Biol 13:192. https://doi.org/10.1186/1471-2148-13-192
O’rr GA, Presgraves DC (2000) Speciation by postzygotic isolation: forces, genes and molecules. BioEssays 22:1085–1094. https://doi.org/10.1002/1521-1878
Odierna G, Aprea G, Capriglione T, Puky M (2004) Chromosomal evidence for the double origin of viviparity in the European common lizard Lacerta (Zootoca) vivipara. Herpetol J 14:157–160
Odierna G, Heulin B, Guillaume CP, Vogrin N, Aprea G, Capriglione T et al. (2001) Evolutionary and biogeographical implications of the karyological variations in the oviparous and viviparous forms of Lacerta vivipara. Ecography 24:332–340. https://doi.org/10.1034/j.1600-0587.2001.240311.x
Pfennig DW, Pfennig KS (2012) Evolution’s wedge: competition and the origins of diversity. University of California Press, Berkeley, CA
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Qualls CP, Shine R (2006) Lerista bougainvillii, a case study for the evolution of viviparity in reptiles. J Evol Biol 11:63–78. https://doi.org/10.1046/j.1420-9101.1998.11010063.x
Ridley M (2004) Evolution. Blackwell Publishing, Oxford, UK
Rodriguez-Prieto A, Giovine G, Laddaga L, Ghielmi S, Cornetti L (2017) Very similar, but not identical: morphological taxonomic identification to improve the resoution of fine-scale distribution of Zootoca (vivipara) carniolica. Amphib-Reptil 38:533–539. https://doi.org/10.1163/15685381-00003120
San-Jose LM, Peñalver-Alcázar M, Milá B, Gonzalez-Jimena V, Fitze PS (2014) Cumulative frequency-dependent selective episodes allow for rapid morph cycles and rock-paper-scissors dynamics in species with overlapping generations. Proc R Soc B 281:20140976. https://doi.org/10.1098/rspb.2014.0976
Smith SA, Shine R (1997) Intraspecific variation in reproductive mode within the scincid lizard Saiphos equalis. Aust J Zool 45:435–445
Surget-Groba Y, Heulin B, Guillaume CP, Thorpe RS, Kupriyanova L, Bogrin N et al. (2001) Intraspecific phylogeography of Lacerta vivipara and the evolution of viviparity. Mol Phylogenet Evol 18:449–459. https://doi.org/10.1006/mpev.2000.0896
Takeuchi H, Zhu GX, Ding L, Tang Y, Ota H, Mori A et al (2014) Taxonomic Validity and Phylogeography of the East Eurasian Natricine Snake, (Berthold, 1859) (Serpentes: Colubridae), as Inferred from Mitochondrial DNA Sequence Data Current Herpetology 33:148–153
Velo-Antón G, Santos X, Sanmartín-Villar I, Cordero-Rivera A, Buckley D (2015) Intraspecific variation in clutch size and maternal investment in pueriparous and larviparous Salamandra salamandra females. Evol Ecol 29:185–204. https://doi.org/10.1007/s10682-014-9720-0
Wake MH (2015) Fetal adaptations for viviparity in amphibians. J Morphol 276:941–960. https://doi.org/10.1002/jmor.20271
Wasserman M, Koepfer HR (1977) Character displacement for sexual isolation between Drosophila mojavensis and Drosophila arizonensis. Evolution 31:812–823
J.L.H. was supported by a Spanish MINECO postdoc grant IJCI-2015-23618. D.L. was supported by the German Academic Exchange Service. Project funds were provided by the Swiss National Science Foundation (PPOOP3_128375, PP00P3_152929/1 to P.S.F.) and the Spanish Ministry of Education and Science (CGL2008-01522, CGL2012-32459, CGL2016-76918 to P.S.F.). A special thank goes to María Luisa Peláez Aller and Teresa Suárez for help with the molecular analyses, Werner Mayer and the Central Research Laboratories of the Natural History Museum Vienna for help with sample collection, and Victoria Gonzalez Cascon (GIS Laboratory of the MNCN) who helped elaborating Figure 1.
Conflict of interest
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