Increased fire frequency promotes stronger spatial genetic structure and natural selection at regional and local scales in Pinus halepensis Mill

Abstract

Background and aims: The recurrence of wildfires is predicted to increase due to global climate change, resulting in severe impacts on biodiversity and ecosystem functioning. Recurrent fires can drive plant adaptation and reduce genetic diversity; however, the underlying population genetic processes have not been studied in detail. In this study, the neutral and adaptive evolutionary effects of contrasting fire regimes were examined in the keystone tree species Pinus halepensis Mill. (Aleppo pine), a fire-adapted conifer. The genetic diversity, demographic history and spatial genetic structure were assessed at local (within-population) and regional scales for populations exposed to different crown fire frequencies.

Methods: Eight natural P. halepensis stands were sampled in the east of the Iberian Peninsula, five of them in a region exposed to frequent crown fires (HiFi) and three of them in an adjacent region with a low frequency of crown fires (LoFi). Samples were genotyped at nine neutral simple sequence repeats (SSRs) and at 251 single nucleotide polymorphisms (SNPs) from coding regions, some of them potentially important for fire adaptation.

Key results: Fire regime had no effects on genetic diversity or demographic history. Three high-differentiation outlier SNPs were identified between HiFi and LoFi stands, suggesting fire-related selection at the regional scale. At the local scale, fine-scale spatial genetic structure (SGS) was overall weak as expected for a wind-pollinated and wind-dispersed tree species. HiFi stands displayed a stronger SGS than LoFi stands at SNPs, which probably reflected the simultaneous post-fire recruitment of co-dispersed related seeds. SNPs with exceptionally strong SGS, a proxy for microenvironmental selection, were only reliably identified under the HiFi regime.

Conclusions: An increasing fire frequency as predicted due to global change can promote increased SGS with stronger family structures and alter natural selection in P. halepensis and in plants with similar life history traits.

Keywords: Genetic diversity; demographic history; fire ecology; natural selection; spatial genetic structure.

Fig. 1.

Study stands of Pinus halepensis in the Eastern Iberian Peninsula belong to different ecoregions. Coastal stands experience a high frequency of crown fires (HiFi) while inland stands experience a low frequency (LoFi).

Fig. 2.

Plot of F_ST as a function of heterozygosity at SNP loci, as determined in a hierarchical island model contrasting HiFi and LoFi stands. Three F_ST outliers lie well above the 99 % confidence envelope.

Fig. 3.

Spatial genetic structure in P. halepensis stands using SSRs and SNPs. The average kinship coefficient F_D was plotted against the logarithm of the geographic distance classes between individuals. The colours of the curve indicate the fire regime, grey for low crown fire frequency (LoFi) and black for high crown fire frequency (HiFi); the symbols indicate the sample location. Significance of the SGS pattern is indicated by continuous lines (P < 0·05), marginal significance by a dashed line (P < 0·1) and non-significance by dotted lines. S. Calderona, Serra Calderona.

Fig. 4.

SGS estimates expressed as mean jackknife regression slopes b and their 95 % confidence intervals (CIs); a negative regression slope with CIs not overlapping zero indicates significant SGS. (A) Within-stand SGS across all Pinus halepensis HiFi (black symbols) or LoFi (grey symbols) stands. HiFi stands had stronger SGS (more negative b) than LoFi stands at SNPs but not at SSRs. (B) Comparison of observed SGS between SSRs and SNPs by population. In the HiFi stands of Alzira and Serra Calderona, non-overlapping CIs between markers suggest that different evolutionary processes operate on SSRs vs. SNPs. S. d’Irta, Serra d’Irta; S. Calderona, Serra Calderona.