Influence of Pliocene and Pleistocene climates on hybridization patterns between two closely related oak species in China

Abstract

Background and aims: Contemporary patterns of genetic admixture reflect imprints of both ancient and recent gene flow, which can provide us with valuable information on hybridization history in response to palaeoclimate change. Here, we examine the relationships between present admixture patterns and past climatic niche suitability of two East Asian Cerris oaks (Quercus acutissima and Q. chenii) to test the hypothesis that the mid-Pliocene warm climate promoted while the Pleistocene cool climate limited hybridization among local closely related taxa.

Methods: We analyse genetic variation at seven nuclear microsatellites (1111 individuals) and three chloroplast intergenic spacers (576 individuals) to determine the present admixture pattern and ancient hybridization history. We apply an information-theoretic model selection approach to explore the associations of genetic admixture degree with past climatic niche suitability at multiple spatial scales.

Key results: More than 70 % of the hybrids determined by Bayesian clustering analysis and more than 90 % of the individuals with locally shared chloroplast haplotypes are concentrated within a mid-Pliocene contact zone between ~30°N and 35°N. Climatic niche suitabilities for Q. chenii during the mid-Pliocene Warm Period [mPWP, ~3.264-3.025 million years ago (mya)] and during the Last Glacial Maximum (LGM, ~0.022 mya) best explain the admixture patterns across all Q. acutissima populations and across those within the ancient contact zone, respectively.

Conclusions: Our results highlight that palaeoclimate change shapes present admixture patterns by influencing the extent of historical range overlap. Specifically, the mid-Pliocene warm climate promoted ancient contact, allowing widespread hybridization throughout central China. In contrast, the Pleistocene cool climate caused the local extinction of Q. chenii, reducing the probability of interspecific gene flow in most areas except those sites having a high level of ecological stability.

Keywords: Quercus acutissima; Quercus chenii; China; Pleistocene; Pliocene; genetic admixture pattern; hybridization; introgression; palaeoclimate.

Fig. 1.

Results of STRUCTURE, PCA, NewHybrids and INTROGRESSION analyses based on the genetic variation at seven nuclear microsatellite loci. (A) Geographical distributions of two genetic clusters corresponding to Quercus acutissima (blue) and Q. chenii (orange) as inferred by STRUCTURE analyses. Circle area is proportional to the sample size. (B) Number of putative hybrids at each site. In A and B, orange and green areas indicate the climatically suitable areas for Q. chenii during the mid-Pliocene Warm Period (mPWP) and during the present, respectively. They were created from the logistic outputs of MAXENT using the maximum sensitivity plus specificity threshold (Gugger et al., 2013). Population codes (Q. acutissima: 1–30; Q. chenii: 31–48) are described in Supplementary Data Table S1. *Populations inside the ancient contact zone. (C) Histogram of an individual’s probability of assignment to Q. acutissima (blue) and Q. chenii (orange) in STRUCTURE analyses. Each vertical bar represents one individual. (D) PCA result for Q. acutissima, Q. chenii and their hybrids. (E) Posterior probability (PP) assigned to Q. acutissima for parental individuals of Q. acutissima (group PA, n = 642) and hybrids morphologically assigned to Q. acutissima (group HA, n = 54), and to Q. chenii for parental individuals of Q. chenii (group PC, n = 395) and hybrids morphologically assigned to Q. chenii (group HC, n = 20). The PP values are averaged over ten independent runs of NewHybrids analyses. (F) Maximum-likelihood hybrid index (H) estimated by the R package introgression for the PA, HA, HC and PC groups.

Fig. 2.

Four demographic scenarios tested by approximate Bayesian computation (ABC): strict isolation (SI), isolation with migration (IM), ancient migration (AM) and secondary contact (SC). N_ACU, N_CHE and N_ANC are effective population sizes of Quercus acutissima, Q. chenii and their ancestor, respectively. T_DIV is the number of generations since the initial divergence. T_AM is the number of generations since the two species stopped exchanging alleles. T_SC is the number of generations since the two species began exchanging alleles. Dark grey arrows denote the effective migration rate from Q. acutissima to Q. chenii (4N_CHEm_A→C) and that in the opposite direction (4N_ACUm_C→A).

Fig. 3.

MAXENT prediction maps showing the climatically suitable areas of Quercus acutissima (A–D) and Q. chenii (E–H) during the mid-Pliocene Warm Period (mPWP), Marine Isotope Stage 19 (MIS19) in the Pleistocene, Last Glacial Maximum (LGM) and the present. Plus signs represent the sampling sites of Q. chenii. Solid and open dots represent the sampling sites of Q. acutissima inside and outside the ancient contact zone, respectively.

Fig. 4.

Spatial interpolation for the probability of membership of each Quercus acutissima population to the Q. chenii genetic cluster (Q_CHE) as inferred by STRUCTURE analyses. The interpolated surface was obtained using the inverse distance-weighted method in ArcGIS 10.3 (ESRI). Plus signs represent the sampling sites of Q. chenii. Solid and open dots represent the sampling sites of Q. acutissima inside and outside the ancient contact zone, respectively.

Fig. 5.

Distribution of ancestry estimates in the ancient contact zone (A) and two sympatric populations of Quercus acutissima and Q. chenii, i.e. populations 23 and 45 (AQY and CQY) (B), and populations 30, 42 and 43 (AWTM, CWTM and CZN; see Fig. 1) (C). The ancestry is based on the probability of membership to the genetic cluster of Q. acutissima (Q_ACU). Hartigans’ dip statistic D and its P value were computed using the R package diptest. Colours of bars represent four groups: parental individuals of Q. acutissima (group PA, blue), parental individuals of Q. chenii (group PC, orange), hybrids morphologically assigned to Q. acutissima (group HA, green) and hybrids morphologically assigned to Q. chenii (group HC, red).

Fig. 6.

Geographical distribution (A) and median-joining network (B) of 29 chloroplast DNA haplotypes of Quercus acutissima and Q. chenii. (A) Circle size is proportional to the sample size. Orange and green areas indicate the climatically suitable areas for Q. chenii during the mid-Pliocene Warm Period (mPWP) and during the present, respectively. They were created from the logistic outputs of MAXENT using the maximum sensitivity plus specificity threshold (Gugger et al., 2013). Population codes (Q. acutissima: 1–30; Q. chenii: 31–48) are described in Supplementary Data Table S1. *Populations inside the ancient contact zone. (B) Circle size is proportional to the frequency of a haplotype across all populations. Small black dots indicate inferred intermediate haplotypes not detected in this investigation. Numbers in brackets on branches indicate the number of mutations between haplotypes when branches represent more than one mutation. Three outgroups include Q. phillyraeoides (phi.; GenBank accession number MK105462; Pang et al., 2019), Q. dolicholepis (dol.; KU240010; Yang et al., 2016) and Q. baronii. (bar.; KT963087; Yang et al., 2017). *The haplotypes shared by the two species.