title: Local effects drive heterozygosity-fitness correlations in an outcrossing long-lived tree.
abstract: Heterozygosity-fitness correlations (HFCs) have been used to understand the complex interactions between inbreeding, genetic diversity and evolution. Although frequently reported for decades, evidence for HFCs was often based on underpowered studies or inappropriate methods, and hence their underlying mechanisms are still under debate. Here, we used 6100 genome-wide single nucleotide polymorphisms (SNPs) to test for general and local effect HFCs in maritime pine (Pinus pinaster Ait.), an iconic Mediterranean forest tree. Survival was used as a fitness proxy, and HFCs were assessed at a four-site common garden under contrasting environmental conditions (total of 16 288 trees). We found no significant correlations between genome-wide heterozygosity and fitness at any location, despite variation in inbreeding explaining a substantial proportion of the total variance for survival. However, four SNPs (including two non-synonymous mutations) were involved in significant associations with survival, in particular in the common gardens with higher environmental stress, as shown by a novel heterozygosity-fitness association test at the species-wide level. Fitness effects of SNPs involved in significant HFCs were stable across maritime pine gene pools naturally growing in distinct environments. These results led us to dismiss the general effect hypothesis and suggested a significant role of heterozygosity in specific candidate genes for increasing fitness in maritime pine. Our study highlights the importance of considering the species evolutionary and demographic history and different spatial scales and testing environments when assessing and interpreting HFCs.
authors.affiliation: Department of Forest Ecology and Genetics, Forest Research Centre, INIA, Carretera A Coruña km 7.5, Madrid 28040, Spain.
authors.forename: Isabel
authors.initials: I
authors.lastname: Rodríguez-Quilón
authors.affiliation: Department of Ecology and Evolution, University of Lausanne, Biophore Building, Lausanne 1015, Switzerland.
authors.forename: Luis
authors.initials: L
authors.lastname: Santos-del-Blanco
authors.affiliation: Department of Forest Ecology and Genetics, Forest Research Centre, INIA, Carretera A Coruña km 7.5, Madrid 28040, Spain.
authors.forename: Delphine
authors.initials: D
authors.lastname: Grivet
authors.affiliation: Department of Forest Ecology and Genetics, Forest Research Centre, INIA, Carretera A Coruña km 7.5, Madrid 28040, Spain Department of Evolutionary Ecology, Institute of Ecology, Universidad Nacional Autónoma de México, AP 70-275, México D.F., Mexico.
authors.forename: Juan Pablo
authors.initials: JP
authors.lastname: Jaramillo-Correa
authors.affiliation: CETEMAS-SERIDA, Sección Forestal, Finca Experimental La Mata, Grado 33820, Spain.
authors.forename: Juan
authors.initials: J
authors.lastname: Majada
authors.affiliation: Institute of Biosciences and Bioresources, National Research Council, Sesto Fiorentino (Florence) 50019, Italy.
authors.forename: Giovanni G
authors.initials: GG
authors.lastname: Vendramin
authors.affiliation: Department of Forest Ecology and Genetics, Forest Research Centre, INIA, Carretera A Coruña km 7.5, Madrid 28040, Spain Sustainable Forest Management Research Institute, University of Valladolid-INIA, Palencia 34071, Spain.
authors.forename: Ricardo
authors.initials: R
authors.lastname: Alía
authors.affiliation: Department of Forest Ecology and Genetics, Forest Research Centre, INIA, Carretera A Coruña km 7.5, Madrid 28040, Spain INRA, UMR 1202 Biodiversité Gènes Ecosystèmes (Biogeco), Cestas 33610, France Université de Bordeaux, UMR 1202 Biodiversité Gènes Ecosystèmes (Biogeco), Talence 33170, France santiago.gonzalez-martinez@pierroton.inra.fr.
authors.forename: Santiago C
authors.initials: SC
authors.lastname: González-Martínez
mesh_terms: D005075:Biological Evolution; D056084:Genetic Fitness; D014644:Genetic Variation; D018745:Genome, Plant; D055106:Genome-Wide Association Study; D006579:Heterozygote; D028223:Pinus / Q000235:genetics*; D020641:Polymorphism, Single Nucleotide
keywords: adaptation; genetic variation; maritime pine; single nucleotide polymorphism; survival