Range-wide genetic structure of maritime pine predates the last glacial maximum: evidence from nuclear DNA

Abstract

Using nuclear simple sequence repeats (nuSSRs), we determined the genetic variability in the natural distribution range of maritime pine (Pinus pinaster) in the western Mediterranean region. We analysed the role of global and significant climatic fluctuations in driving the evolutionary diversification of this species. We attempted to determine the impact of the last glacial maximum (LGM) and human activity on genetic variation and to identify the effect of bottlenecks, admixing, migration, time to the most recent common ancestor (TMRCA), and recent splits. A total of 972 individuals were analysed. The sample represented 27 natural populations from the western Mediterranean region, which encompasses most of the natural range of P. pinaster. Using eight nuSSRs, we analysed genetic diversity indices for each population and group of populations. We also examined the interpopulation structure by the frequency and distance method and investigated genetic barriers, signals of historical demographic fluctuations, phylogeographic structure, admixing, rate of mutation, migration, as well as testing the hypothesis of isolation by distance (IBD). Both cluster analyses showed similar population genetic structure with three genetic barriers that divided the samples into four large groups. Intensive migration was only detected during the period of the last glacial maximum (LGM), which permitted the mutation rate of the markers used to be calculated. The majority of the population was found to exhibit signs of a recent bottleneck and its timing showed a clear northeast-southwest geographic distribution. A clearly defined phylogeographic structure (Nst > Gst and Rst > Gst ) under IBD was established, and showed the highest divergence between groups of populations separated by physical barriers, such as the Strait of Gibraltar, the Mediterranean Sea and the Pyrenees. The high level of intergroup genetic differentiation (ΦIS = 20.26) was attributed to a long historical isolation (which occurred before the last 18 000 years) between the principal maritime pine population groups that occurred due to physical barriers that limited pollen and seed transfer, combined with a minimal effective radius of distribution. The low level of genetic diversity among the populations was combined with genetic drift and a recent bottleneck during the period of human activity. Significant migration across barriers was due to spontaneous phenomena during the LGM, which had no significant impact on the genetic structure owing to its relatively short duration and the fragmented species. The phylogeographic structure under the assumption of IBD was well established for P. pinaster in each of the principal population groups.

Local effects drive heterozygosity–fitness correlations in an outcrossing long-lived tree

“…3 in [29]; see also [37]). Based on molecular markers, six extant gene pools have been described in the species (French Atlantic coast, Iberian Atlantic coast, central Spain, southern Spain, Corsica and Morocco [38,39]; figure 1), which also showed evidence of genetic differentiation for adaptive traits [38,40].…”

“…However, when compared with other Pinus species, maritime pine has reduced inbreeding depression (although still significant), in particular for fecundity traits and general vigour [60]. Evidence of historical demographic bottlenecks in the species [29,37] suggests that some genetic load may have been purged during maritime pine survival in isolated glacial refugia [2,28,61,62], contributing to the observed lack of general effect HFCs [5,17,28,63]. This hypothesis is supported by a relatively low correlation between heterozygosity and inbreeding (r 2 ¼ 0.17), which renders HFCs non-significant despite a substantial proportion of the total variance in survival being explained by variation in inbreeding (22-51%, depending on common garden).…”

High rate of adaptive evolution in two widespread European pines

“…This conifer grows in warm temperate regions with an oceanic influence on climate (Abad Viñas, Caudullo, de Oliveira, & de Rigo, ) and is particularly well adapted to dry and fire‐prone environments. Its demographic history is characterized by a more recent bottleneck relative to Scots pine (Naydenov et al., ), and it has a strong genetic structure among populations across its range (Bucci et al., ; Burban & Petit, ; Jaramillo‐Correa et al., ) that is accompanied by morphological and physiological differences (Alía, Gil, & Pardos, ; Corcuera, Gil‐Pelegrín, & Notivol, ; Kremer & Roussel, ; Lamy et al., ; Santos‐del‐Blanco et al., ), defining various subspecies and ecotypes (Richardson ). This genetic structure likely results from post‐Pleistocene events (Bucci et al., ; Burban & Petit, ; Naydenov et al., ), including adaptation to local climate (Serra‐Varela et al., ).…”

Ecological and association genetics in two Mediterranean pine species

“…where it presumably overcame severe bottlenecks (see Fig.3 in and Naydenov et al (2014) ; see figure 1), which also showed evidence of genetic differentiation for adaptive traits (González-Martínez et al 2002;. High molecular and phenotypic variability among gene pools, together with population adaptive divergence, make maritime pine particularly interesting for HFCs studies at different spatial scales.…”

“…However, when compared to other Pinus species, maritime pine has reduced inbreeding depression (although still significant), in particular for fecundity traits and general vigour (Durel et al 1996). Evidence of historical demographic bottlenecks in the species Naydenov et al 2014) suggests that some genetic load may have been purged during maritime pine survival in isolated glacial refugia (Byers and Waller 1999;Richardson et al 2004;Charlesworth and Willis 2009), contributing to the observed lack of general effect HFCs (Byers and Waller 1999;Frankham 2001, 2003;Chapman et al 2009). This hypothesis is supported by a relatively low correlation between heterozygosity and inbreeding (r2=0.17), which renders…”