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Red deer in Iberia: Molecular ecological studies in a southern refugium and inferences on European postglacial colonization history - PubMed

  • ️Tue Jan 01 2019

Red deer in Iberia: Molecular ecological studies in a southern refugium and inferences on European postglacial colonization history

João Queirós et al. PLoS One. 2019.

Abstract

The red deer (Cervus elaphus) is a widespread wild ungulate in Europe that has suffered strong anthropogenic impacts over their distribution during the last centuries, but also at the present time, due its economic importance as a game species. Here we focus on the evolutionary history of the red deer in Iberia, one of the three main southern refugial areas for temperate species in Europe, and addressed the hypothesis of a cryptic refugia at higher latitudes during the Last Glacial Maximum (LGM). A total of 911 individuals were sampled, genotyped for 34 microsatellites specifically developed for red deer and sequenced for a fragment of 670 bp of the mitochondrial (mtDNA) D-loop. The results were combined with published mtDNA sequences, and integrated with species distribution models and historical European paleo-distribution data, in order to further examine the alternative glacial refugial models and the influence of cryptic refugia on European postglacial colonization history. Clear genetic differentiation between Iberian and European contemporary populations was observed at nuclear and mtDNA levels, despite the mtDNA haplotypes central to the phylogenetic network are present across western Europe (including Iberia) suggesting a panmictic population in the past. Species distribution models, fossil records and genetic data support a timing of divergence between Iberian and European populations that overlap with the LGM. A notable population structure was also found within the Iberian Peninsula, although several populations displayed high levels of admixture as a consequence of recent red deer translocations. Five D-loop sub-lineages were found in Iberia that belong to the Western European mtDNA lineage, while there were four main clusters based on analysis of nuclear markers. Regarding glacial refugial models, our findings provide detailed support for the hypothesis that red deer may have persisted in cryptic northern refugia in western Europe during the LGM, most likely in southern France, southern Ireland, or in a region between them (continental shelf), and these regions were the source of individuals during the European re-colonization. This evidence heightens the importance of conserving the high mitochondrial and nuclear diversity currently observed in Iberian populations.

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Conflict of interest statement

We have the following interests. MB has a current affiliation with SABIOtec. SABIOtec did not intervene in experimental design, data collection and analysis. There are no patents, products in development or marketed products to declare. This does not alter our adherence to all the PLOS ONE policies on sharing data and materials, as detailed online in the guide for authors.

Figures

Fig 1
Fig 1. Location and management regime (within the Iberian Peninsula) of red deer populations sampled in this study (population code in brackets): 1-Asturias (ASR); 2-Cantabria (CTR); 3-Huesca (HUR); 4-El Berguedà (BER); 5-Parque Natural de Montesinho/Sierra Culebra (PMC); 6-Burgos (BUR); 7-Caspe-Fraga (CFR); 8-Parque Natural do Alto Tajo (PNA); 9-Serra da Lousa (SLR); 10-Parque Natural do Tejo Internacional (PNB); 11-Parque Nacional de Monfragüe (PNM); 12/20-Montes de Toledo region (MTR): 12-MT1, 13-MT2, 14-Parque Nacional Cabañeros (PNC), 15-MT3, 16-MT4, 17-MT5, 18-MT6, 19-Quintos de Mora estate (QMS) and 20-MT7; 21/26-Sierra Morena region (SMR): 21-SM1, 22-SM2, 23-SM3, 24-SM4, 25-SM5 and 26-SM6; 27-Moura/Barrancos (MBR); 28-Parque Natural Sierra de Aracena y Picos de Aroche (PNP); 29-Parque Nacional Doñana (PND); 30-Parque Natural de Sierra de Grazalema (PNS); 31-England (EN); 32-France (FR); 33-Switzerland (SW); 34-Italy (IT); 35-Norway (NO); 36-Sweden (SE); 37-Czech Republic (CZ); and 38-Hungary (HU).

The red deer distribution range in western Europe used for modelling purposes is shown in light grey [16], while the Iberian red deer distribution around 1970 is represented in dark grey [39].

Fig 2
Fig 2

Putative scenarios of divergence (for 3 different times: t1, t2 and t3) among (a) European red deer populations (Iberian—IB, French—FR, English–EN, Norwegian–NO, Swedish–SE, Czech–CZ and Hungarian–HU) and (b) the Iberian populations (Montes de Toledo region–MTR, Parque Natural de Tejo Internacional–PNB, Sierra Morena region–SMR and Caspe/Fraga region–CFR;) tested using Approximate Bayesian Computation (ABC) analyses implemented in DIYABC 2.0. Details about the individuals included on the Iberian populations are depicted in the Material and methods section.

Fig 3
Fig 3. Population genetic structure of the Iberian and European red deer using microsatellite data.

a) Bayesian clustering analyses conducted in STRUCTURE and considering the best ΔK value (ΔK = 2). Individual membership proportion to each cluster is indicated in grey for the Iberian populations and black for the central and northern European populations (see details S1 Fig); b) and c) Plots showing the results of the Factorial Correspondence Analysis–b) components 1 and 2, c) components 1 and 3. A red arrow highlights the individual identified (in BER population) as belonging to the European cluster. Population codes are described as in Fig 1.

Fig 4
Fig 4. Population genetic structure in the Iberian red deer using microsatellite data.

a) Bayesian clustering analyses conducted in STRUCTURE and considering the highest ΔK value (ΔK = 3). Individual membership proportion to each cluster is indicated in light grey for the Montes de Toledo cluster, grey for the Sierra Morena cluster and dark grey for the Fraga/Caspe cluster (see details S1 Fig); b) and c) Plots showing the results of the Factorial Correspondence Analysis. The population from Parque Natural Tejo Internacional (PNB) was distinctive as well as the three aforementioned clusters–b) components 1 and 2, c) components 1 and 3. Population codes are described as in Fig 1. These analyses excluded the individuals sampled in the Iberian Peninsula that showed a membership proportion lower than 95% for the Iberian cluster in the European analysis and those individuals that had the mtDNA haplotype 11 (n = 73, see details S12 Table).

Fig 5
Fig 5. Median joining network showing the evolutionary relationship of mtDNA D-loop haplotypes found both in this study and those published in GenBank (329 bp fragment size) for the red deer in Europe.

A bar in each solid line represents a mutational step; small black circles show undetected/extinct intermediate haplotype states; color codes within the circles are depicted for Western European lineage (haplogroup A) and represent the country where the haplotypes were found. The Iberian sub-lineages are grouped by colored shading following Fig 6. GenBank accession numbers of the 509 original haplotypes used in this analysis, as well as their correspondent haplotypes for 329 bp (represented by numbers within circles) are given in S1 Table.

Fig 6
Fig 6. Gene genealogy and phylogenetic relationships of the red deer in the Iberian Peninsula using mtDNA D-loop fragment (650 bp).

a) Median joining network showing the evolutionary relationship and the frequency of the Iberian haplotypes reported in this study. Haplotypes described distinctively in Carranza et al. [33] are depicted as small grey circles, while haplotypes reported in both studies are highlighted as circle thick line. Colour codes represent the various evolutionary sub-lineages reported in this study, including the central haplotypes, as represented in Fig 5. A bar in each solid line represents a mutational step; small black circles show undetected/extinct intermediate haplotype states. b) Distribution pattern of the evolutionary sub-lineages across Iberia. Color codes in the pie graphics represent the proportion of each sub-lineage by population.

Fig 7
Fig 7. Bayesian Skyline Plots of the effective population size of red deer through time estimated from post-burn-in generations from two MCMC simulations, based on mtDNA data.

The black line is the logarithm of median effective population size, log Ne. The grey area bordered by dashed lines represent the 95% highest posterior density limits. a) Iberian haplotypes found in this study. b) British Isles haplotypes reported by Peréz-Espona et al. [71] and McDevitt et al. [68].

Fig 8
Fig 8. Climatic suitability for occurrence of red deer at 6 ky BP, 22 ky BP and 120 ky BP—according to the climatic niche for the species determined by GLM.
Fig 9
Fig 9. The red deer fossil records dated throughout the last 50 ky BP in Europe.

a) the sampling locations were organized according to the favorable areas predicted by the 22 ky BP species distribution model: central-northern Europe, CN-EU; south-west France, SW-FR; south-east France, SE-FR; British Isles, BI; Italy, IT; East Europe, E-EU; west Iberian Peninsula, W-IP; north Iberian Peninsula, N-IP; south-east Iberian Peninsula, SE-IP; b) plot showing the presence of fossil red deer records directly (orange) or indirectly (grey) dated for each area identified above. Dotted lines represent the LGM interval (26.5 to 19 Ky BP) [110].

Fig 10
Fig 10. Timeframe of the evolutionary and demographic history of red deer in Europe proposed in this study, since 190 thousand years before present (ky BP) to the present time.

The colored arrows in the graphics correspond to the biogeographical events summarized in the time-line. The divergence time inferred using the nuclear and mitochondrial data are also highlighted at the European and Iberian levels.

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This work was supported by: Portuguese national funds through the FCT (Fundação para a Ciência e a Tecnologia), FEDER funds (Fundo Europeu de Desenvolvimento Regional) through Programa Operacional Potencial Humano-Quadro de Referência Estratégico Nacional (POPH-QREN) from the European Social Fund and Portuguese Ministério da Educação e Ciência and the project ‘Genomics applied to genetic resources’, North Portugal Regional Operational Programme 2007/2013 (ON.2 – O Novo Norte); the EU grant ‘Harmonised approaches in monitoring wildlife population health, and ecology and abundance’ (APHAEA, 219235_FP7_ERA-NET_EMIDA) and CDTI. This is also a contribution to grant AGL20111-30041 from MINECO, Spain. MB is currently an employee and CEO of SABIOtec commercial company. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript and only provided financial support in the form of grants to the authors (SFRH/BD/73732/2010 PhD grant to JQ, SFRH/BD/5880/2008 PhD grant to JPVS and SFRH/BSAB/1278/2012 sabbatical grant to PCA) and/or research materials.