Spatial Genetic Structure of a Symbiotic Beetle-Fungal System: Toward Multi-Taxa Integrated Landscape Genetics

Patrick M A James,Richard C Hamelin,Dave W Coltman,Felix A H Sperling,Brent W Murray,Simon Joly

doi:10.1371/journal.pone.0025359

Abstract

Spatial patterns of genetic variation in interacting species can identify shared features that are important to gene flow and can elucidate co-evolutionary relationships. We assessed concordance in spatial genetic variation between the mountain pine beetle (Dendroctonus ponderosae) and one of its fungal symbionts, Grosmanniaclavigera, in western Canada using neutral genetic markers. We examined how spatial heterogeneity affects genetic variation within beetles and fungi and developed a novel integrated landscape genetics approach to assess reciprocal genetic influences between species using constrained ordination. We also compared landscape genetic models built using Euclidean distances based on allele frequencies to traditional pair-wise Fst. Both beetles and fungi exhibited moderate levels of genetic structure over the total study area, low levels of structure in the south, and more pronounced fungal structure in the north. Beetle genetic variation was associated with geographic location while that of the fungus was not. Pinevolume and climate explained beetle genetic variation in the northern region of recent outbreak expansion. Reciprocal genetic relationships were only detectedin the south where there has been alonger history of beetle infestations. The Euclidean distance and Fst-based analyses resulted in similar models in the north and over the entire study area, but differences between methods in the south suggest that genetic distances measures should be selected based on ecological and evolutionary contexts. The integrated landscape genetics framework we present is powerful, general, and can be applied to other systems to quantify the biotic and abiotic determinants of spatial genetic variation within and among taxa.

Highlights

The current mountain pine beetle (MPB; Dendroctonusponderasae) outbreak in western Canada is unprecedented in terms of extent and severity and has had significant ecological and economic consequences [1,2]
Landscape Genetics After characterizing genetic structure in both species, we investigated whether landscape features could explain further marginal variation in allele frequencies among landscapes using redundancy analysis (RDA), a form of constrained ordination
In the south we found some evidence for significant reciprocal genetic influences, these influences were not symmetrical between methods: the fungus helped explain the beetle using RDA, but beetles helped explain the fungus using distance-based redundancy analysis (dbRDA)

Summary

Introduction

The current mountain pine beetle (MPB; Dendroctonusponderasae) outbreak in western Canada is unprecedented in terms of extent and severity and has had significant ecological and economic consequences [1,2]. The mountain pine beetlehas a symbiotic relationship with several fungi in the Ophiostomataceaefamily [7] These fungi provide benefits to the beetle including larvalnutrition, protection from tree defenses, and stressing attacked trees to facilitate beetle mass attack [5,8,9]. Otherstudies have compared the contemporary genetic structure of interacting species including termites and symbiotic fungi [13], ants and their cultivated fungi [14], and other host-parasitoid interactions [15]. Few of these studies have compared contemporary genetic variation of symbionts in a spatially explicit context, the importance of spatial heterogenetiy to species interactions and coevolution is well accepted [15,16]

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