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.

Telomere length reveals cumulative individual and transgenerational inbreeding effects in a passerine bird

“…These parameters are comparable to that reported in other organisms including trees (Rodríguez‐Quilón et al . ) and mammals (Annavi et al . ).…”

Evidence of opposing fitness effects of parental heterozygosity and relatedness in a critically endangered marine turtle?

“…With the widespread use of microsatellite markers for HFC studies, this discussion has focussed on the relative roles of ‘general’ and ‘local’ effects (e.g. Hansson & Westerberg, ; Rodriguez‐Quilon et al ., ), and the associated question of the link between marker‐based heterozygosity and inbreeding coefficients (e.g. Balloux et al ., ; Berenos et al ., ; Nietlisbach et al ., ), although these models are not mutually exclusive.…”

Demographic history and spatial genetic structure in a remnant population of the subtropical tree Anadenanthera colubrina var. cebil (Griseb.) Altschul (Fabaceae)

“…Despite the high levels of genetic diversity found in our study, we must be cautious when interpreting the intrinsic value of this remnant forest stand (Hedrick 1999). First, genetic diversity as estimated here only refers to neutral genetic diversity and not to variation associated with quantitative traits with adaptive value, and recent studies have shown little correlation between these two measures of diversity (e.g., Rodríguez-Quilón et al 2015). Second, high genetic diversity is accompanied by high levels of inbreeding and differentiated genetic clusters, which also calls for caution in the use of this stand as seed source (Ellstrand and Elam 1993;Charlesworth 2003).…”

“…In long-lived tree species, changes in effective population size, defined as the average number of individuals that contribute offspring to the next generation (Ridley 2003), may be slow and difficult to detect. Moreover, the fact that genetic processes operate in time units of generations may introduce important time lags in the response of forest trees to landscape change, including fragmentation (Wagner and Fortin 2013).…”