New insights into the phylogeny and worldwide dispersion of two closely related nematode species, Bursaphelenchus xylophilus and Bursaphelenchus mucronatus.

Andreas Hejnol,Filipe Pereira,Barbara Van Asch,Cláudia Moreira,António Amorim,Manuel Mota,Isabel Abrantes,Luís Fonseca

doi:10.1371/journal.pone.0056288

Andreas Hejnol, Filipe Pereira + Show 6 more

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https://doi.org/10.1371/journal.pone.0056288

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Abstract

The pinewood nematode, Bursaphelenchus xylophilus, is one of the greatest threats to coniferous forests worldwide, causing severe ecological damage and economic loss. The biology of B. xylophilus is similar to that of its closest relative, B. mucronatus, as both species share food resources and insect vectors, and have very similar morphological characteristics, although little pathogenicity to conifers has been associated with B. mucronatus. Using both nuclear and mitochondrial DNA markers, we show that B. xylophilus and B. mucronatus form distinct phylogenetic groups with contrasting phylogeographic patterns. B. xylophilus presents lower levels of intraspecific diversity than B. mucronatus, as expected for a species that evolved relatively recently through geographical or reproductive isolation. Genetic diversity was particularly low in recently colonised areas, such as in southwestern Europe. By contrast, B. mucronatus displays high levels of genetic diversity and two well-differentiated clades in both mitochondrial and nuclear DNA phylogenies. The lack of correlation between genetic and geographic distances in B. mucronatus suggests intense gene flow among distant regions, a phenomenon that may have remained unnoticed due to the reduced pathogenicity of the species. Overall, our findings suggest that B. xylophilus and B. mucronatus have different demographic histories despite their morphological resemblance and ecological overlap. These results suggest that Bursaphelenchus species are a valuable model for understanding the dispersion of invasive species and the risks posed to native biodiversity and ecosystems.

Highlights

The pinewood nematode (PWN), Bursaphelenchus xylophilus (Nematoda: Aphelenchoididae), is the causal agent of the widespread pine wilt disease (PWD), which causes severe ecological and economic losses in coniferous forests [1,2]
It has been suggested that the ancestor of B. mucronatus and other species of the genus Bursaphelenchus was a free-living nematode inhabiting broad-leaved trees in the eastern part of Eurasia, while B. xylophilus likely originated from a population of B. mucronatus that colonised the North American continent [17]
Mitochondrial haplotypes from isolates of both species were separated by at least 35 mutational steps in the c oxidase subunit I (COI) median-joining network (Figure 2), which is in agreement with previous results on inter-species mitochondrial DNA (mtDNA) phylogeny of Bursaphelenchus [8,17]

Summary

Introduction

The pinewood nematode (PWN), Bursaphelenchus xylophilus (Nematoda: Aphelenchoididae), is the causal agent of the widespread pine wilt disease (PWD), which causes severe ecological and economic losses in coniferous forests [1,2]. We provide new insights into the intraspecific phylogeny of B. xylophilus and B. mucronatus using mitochondrial and nuclear DNA data from isolates of different world regions.

Results

Conclusion