High population differentiation and unusual haplotype structure in a shade‐intolerant pioneer tree species, Zanthoxylum ailanthoides (Rutaceae) revealed by analysis of DNA polymorphism at four nuclear loci

Abstract

Differences in demographic history, life-history traits, and breeding systems affect nucleotide variation patterns. It is expected that shade-intolerant pioneer tree species have different patterns of genetic polymorphism and population structure than climax species. We studied patterns of nucleotide polymorphism at four putative starch pathway loci (agpSA, agpSB, agpL, and GBSSI) in Zanthoxylum ailanthoides, a shade-intolerant pioneer tree species that occupies forest gaps in warm-temperate forests of East Asia. Genetic diversity was lower within each population than among populations, and differentiation among populations was high across the loci (F(ST) = 0.32-0.64), as expected from the insect-pollinated breeding system and the metapopulation structure of this pioneer species. Numbers of haplotypes were smaller than those expected from the observed numbers of segregating sites. Single haplotypes accounted for more than 47% of all the sampled genes at the respective loci. These variation patterns were incompatible with neutral predictions for populations of a finite island model. Complex population dynamics, such as bottleneck and/or admixture, in the history of this pioneer tree species might have resulted in the observed patterns of genetic variation and population structure, which are different from those of climax wind-pollinated tree species, such as conifers. In contrast to the other loci investigated in this study, agpL showed nearly no variation in Z. ailanthoides (one singleton only), but there was some extent of variation in a closely related species, Zanthoxylum schinifolium. This suggests possibly a recent selective sweep at or near the locus in Z. ailanthoides.

Molecular evidence for natural intergeneric hybridization between Liquidambar and Altingia

“…The mean divergence between A. obovata and L. formosana is low, about 3.45 and 1.51% according to the two genes used in this study (Table S3). The level of divergence is comparable with that of two sister species within a single genus (Sang et al 1995;Zhou et al 2007;Kamiya et al 2008). The low level of divergence between Liquidambar and Altingia may indicate that the ease of hybridization between them is equivalent to intrageneric hybridization in other plant groups.…”

Genetic structure and putative selective sweep in the pioneer tree, Zanthoxylum ailanthoides

“…A part of the putative candidate selected gene, agpL, suggested by Kamiya et al (2008) was newly sequenced for five samples each from four populations selected on the basis of their locations (populations with asterisks in Fig. 1).…”

“…It is distributed throughout the east coast of Asia from the Philippines to the main island of Japan and is often found in warm-temperate evergreen oak forests below 1,500 m (Horikawa 1972). We investigated nucleotide sequence variation at four nuclear loci in a limited sample of this species from southern Japan (Kyushu) and observed remarkably high levels of genetic differentiation among populations and low haplotype number (Kamiya et al 2008), both of which were different from those found in many other trees thus far studied (González-Martinez et al 2006;Savolainen and Pyhäjärvi 2007). Furthermore, one of the four loci, agpL, encoding the large subunit of the heterotetrameric enzyme, AGPase, had remarkably low nucleotide diversity (nearly no variation) compared with the other three loci, although the divergence of agpL from that in its sister species was not low.…”

“…Because Z. ailanthoides grows in disturbed areas in Japanese warm-temperate evergreen oak forests, there might have been large populations of this species in southern Kyushu, and populations of warmtemperate evergreen oak trees. But only a few samples were taken from southern Kyushu in Kamiya et al (2008). Therefore, it was necessary to estimate the genetic divergence among populations and compare the level of genetic diversity between the population in hypothetical refugia and other populations using many loci and more widely sampled materials.…”

“…However, in Kamiya et al (2008), 44 individuals from five populations in only a single area, Kyushu Island in southwestern Japan, were investigated using four nuclear loci. Therefore, the wide-range genetic structure was not known and the population differentiation was not accurately estimated because of the small number of loci used.…”