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Downloaded from Brill.Com09/23/2021 01:06:06PM Via Free Access Contributions to Zoology 89 (2020) 270-281 CTOZ brill.com/ctoz Environmental correlates of the European common toad hybrid zone Jan W. Arntzen Naturalis Biodiversity Center, P.O. Box 9517, 2300 RA Leiden, The Netherlands [email protected] Daniele Canestrelli Department of Ecological and Biological Science, Largo dell’Università s.n.c., 01100 Viterbo, Italy [email protected] Iñigo Martínez-Solano Naturalis Biodiversity Center, P.O. Box 9517, 2300 RA Leiden, The Netherlands Department of Biodiversity and Evolutionary Biology, Museo Nacional de Ciencias Naturales, CSIC, c/ José Gutiérrez Abascal 2, 28006 Madrid, Spain [email protected] Abstract The interplay between intrinsic (development, physiology, behavior) and extrinsic (landscape features, climate) factors determines the outcome of admixture processes in hybrid zones, in a continuum from complete genetic merger to full reproductive isolation. Here we assess the role of environmental corre- lates in shaping admixture patterns in the long hybrid zone formed by the toads Bufo bufo and B. spinosus in western Europe. We used species-specific diagnostic SNP markers to genotype 6584 individuals from 514 localities to describe the contact zone and tested for association with topographic, bioclimatic and land use variables. Variables related to temperature and precipitation contributed to accurately predict the distribution of pure populations of each species, but the models did not perform well in areas where genetically admixed populations occur. A sliding window approach proved useful to identify different sets of variables that are important in different sections of this long and heterogeneous hybrid zone, and offers good potential to predict the fate of moving contact zones in global change scenarios. Keywords Bufo bufo – Bufo spinosus – diagnostic SNP markers – France – Italy – two-species distribution model © Arntzen et al., 2019 | doi:10.1163/18759866-bja10001 This is an open access article distributed under the terms of the cc-by 4.0 License. Downloaded from Brill.com09/23/2021 01:06:06PM via free access <UN> Environmental correlates of a hybrid zone 271 Introduction & Rice, 2015; Taylor et al., 2015; Hunter et al., 2017; Ryan et al., 2018). The study of hybrid zones, or areas where in- The European common toad hybrid zone dividuals from two genetically differentiated is an emerging model system in the study of population lineages meet and produce hybrid speciation. The common (Bufo bufo (Linnae- offspring, is critical to our understanding of us, 1758)) and spined (Bufo spinosus Daudin, how new species form and remain distinct 1803) toads meet along a ca. 900 km long hy- through evolutionary time (Barton & Hewitt, brid zone from the Atlantic coast of northwest 1985; Harrison & Larson, 2014). The outcome France to the Mediterranean coast of south- of this admixture process ranges from com- east France and northwest Italy (Recuero plete genetic merger to full reproductive iso- et al., 2012; Arntzen et al., 2018). This hybrid lation with strong selection against hybrid zone has been previously characterized with individuals, and is a result of the interaction mitochondrial and nuclear DNA markers, between intrinsic and extrinsic factors (Mal- which have revealed different patterns of gene- let, 2005; Abbott et al., 2013). Among the for- tic admixture across the hybrid zone, with tran- mer are developmental, physiological and sects in northwestern France resembling a clas- behavioral traits contributing to reproductive sical tension zone model with selection against isolation, whereas extrinsic factors include hybrids and those in the southeast of France those associated with the spatial and climatic and northwest of Italy characterized by strong context of the hybrid zone. cyto-nuclear discordance, probably as a result Hybrid zones often extend for hundreds of of spatial displacement of the hybrid zone in kilometers across heterogeneous landscapes, the past due to climatic changes (Arntzen et al., with features like mountains, rivers, soil types 2016, 2017; van Riemsdijk et al., 2019a, b). or roads differentially restricting dispersal While previous studies have discussed the and, consequentially, the degree of admix- potential role of intrinsic factors in maintain- ture in alternate sections of the contact zone. ing reproductive isolation across the hybrid Similarly, spatially varying climatic conditions zone, the relative role of environmental cor- along the hybrid zone potentially impose relates has not been assessed so far, with the different selective pressures on parental spe- exception of certain topographic features cies and their hybrids in different transects. reported to be associated with genetic transi- While topography is generally more conserved tions in different section of the contact zone through time, climatic changes operate at (Arntzen et al., 2017, 2018). Here we use envi- temporal scales that are relevant for the study ronmental data and a comprehensive genetic of hybrid zone dynamics and have been in- dataset to investigate the role of extrinsic fac- voked to explain patterns of asymmetrical in- tors in maintaining species borders through trogression in moving hybrid zones. The study space and time. of the complex interplay of topographic and climatic factors varying over time and space in hybrid zones can thus illuminate the rela- Materials and methods tive role of extrinsic factors in reproductive isolation, explain discordant genetic patterns A total of 6584 tissue samples was obtained in different sections of a hybrid zone, and help from adult and larval toads from 514 locali- predict the fate of hybrid zones (i.e., the sta- ties across western Europe, with the emphasis bility of reproductive isolation through time) on the broad region of species contact across in the face of climatic changes (McQuillan France and Italy.Downloaded Sampling from Brill.com09/23/2021 was somewhat 01:06:06PM via free access <UN> 272 ARNTZEN et al. sparse at the Atlantic coast and it was unsuc- individual to belong to either cluster on a zero cessful over the lower cols of the French Alps (B. spinosus) to unity scale (B. bufo). In this (col de Montgenèvre at 1854 m a.s.l., colle della mapping exercise data per population were Maddalena at 1996 m, col de Tende at 1870 m). weighted by sample size and by the number All sampled individuals were studied for the of markers employed. We used Dirichlet cells four species-diagnostic SNP nuclear markers with ILWIS (ILWIS, 2009) and linear inter- bdnf, pomc, rag1 and rpl3 (Arntzen et al., 2016). polation with MyStat (Systat, 2007), which Individuals with data missing for more than methods implied a weak and a strong spatial one marker were excluded from the analysis. smoothing, respectively. Population sample size ranged from 1–358, Environmental data considered include with an average of 12.8. A total of 610 individu- altitude and 19 climate variables from the als was studied in duplicate. Results were not WorldClim global climate database v2, avail- the same in two cases (0.08%) and involved able at http://www.worldclim.org (Hijmans the score of ‘22’ (i.e., homozygous for the et al., 2005; see also Fick & Hijmans, 2017). The spinosus-allele) versus the heterozygous ‘12’ parameter ‘slope’ was derived from altitude condition. Both observations were subse- through a set of filter operations. Soil prop- quently treated as unavailable. The total of erties data are from the ESDA European soil missing data was 2.0%. A subset of 2524 in- Database v2.0, available at https://esdac.jrc dividuals from 185 localities was studied for .ec.europa.eu (see also Panagos et al., 2012) another 27 diagnostic SNP markers (as in van and were used as far as parameter values Riemsdijk et al., 2019b; Arntzen, 2019) to de- could be ordered. Vegetation and land use termine the center of the two species contact data were from the CORINE land cover da- zone more accurately. These latter localities tabase of the European Environment Agen- were arranged in eight transects with hybrid cy, available at https://www.eea.europa.eu/ zone centers located in France or Italy. For lo- publications/COR0-landcover. Data were cality information, sample sizes and molecu- grouped in the three classes ‘crop growing’, lar species identifications see supplementary ‘forestation’ and ‘pasture’. table S1. To visualize the locality information To identify and subsequently reduce colin- one can use the given link to the Naturalis de- earity among the environmental variables we pository, and open this .kml file e.g., with Google constructed the half-matrix of their pairwise Earth. Mitochondrial DNA and toad morphol- Pearson correlation coefficients. This matrix ogy were not studied because for these char- was subjected to clustering with UPGMA. acters species diagnostic performances break Variables were retained using criteria of par- down over parts of the species’ parapatric tial independence at r < 0.7 and selected in range border (Arntzen et al., 2017, 2018). alphanumeric order (supplemental fig. S1). The genetic data were subjected to Bayesian The 20 variables considered for the construc- clustering with Structure software (Pritchard tion of species distribution models are listed et al., 2000) with a predetermined K-value of in table 1. two. The position of the mutual range bor- We produced two-species distribution der of B. bufo and B. spinosus was estimated models, in which both species’ environmental by spatial interpolation of Structure Q-values, attributes are contrasted under the assump- to obtain the Q = 0.5 isoline. In the Structure tion of a distribution in parapatry, as follows. analyses K is the number of genetically dif- First, we sampled environmental data for the ferentiated genetic clusters and Q equals the localities of the genetically investigated toad assignment probability for each investigated populations withinDownloaded the area from –5 Brill.com09/23/2021 to 12 degrees 01:06:06PM via free access <UN> Environmental correlates of a hybrid zone 273 Table 1 Environmental variables considered for the construction of two-species distribution models for the common toad B.
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