Genetic and genomic evidence of niche partitioning and adaptive radiation in mountain pine beetle fungal symbionts

Abstract

Bark beetles form multipartite symbiotic associations with blue stain fungi (Ophiostomatales, Ascomycota). These fungal symbionts play an important role during the beetle's life cycle by providing nutritional supplementation, overcoming tree defences and modifying host tissues to favour brood development. The maintenance of stable multipartite symbioses with seemingly less competitive symbionts in similar habitats is of fundamental interest to ecology and evolution. We tested the hypothesis that the coexistence of three fungal species associated with the mountain pine beetle is the result of niche partitioning and adaptive radiation using SNP genotyping coupled with genotype-environment association analysis and phenotypic characterization of growth rate under different temperatures. We found that genetic variation and population structure within each species is best explained by distinct spatial and environmental variables. We observed both common (temperature seasonality and the host species) and distinct (drought, cold stress, precipitation) environmental and spatial factors that shaped the genomes of these fungi resulting in contrasting outcomes. Phenotypic intraspecific variations in Grosmannia clavigera and Leptographium longiclavatum, together with high heritability, suggest potential for adaptive selection in these species. By contrast, Ophiostoma montium displayed narrower intraspecific variation but greater tolerance to extreme high temperatures. Our study highlights unique phenotypic and genotypic characteristics in these symbionts that are consistent with our hypothesis. By maintaining this multipartite relationship, the bark beetles have a greater likelihood of obtaining the benefits afforded by the fungi and reduce the risk of being left aposymbiotic. Complementarity among species could facilitate colonization of new habitats and survival under adverse conditions.

Fungal Frequency and Mite Load Trends Interact with a Declining Mountain Pine Beetle Population

“…It is possible that lethal cool winter temperatures may not be the only limiting factor keeping the beetle outside of these areas. Leptographium longiclavatum has only recently been described from MPB populations in Colorado [39,45], where the beetle's incursions to unusually high elevations were observed during this and another study [75].…”

“…In Colorado, our knowledge comes from the original descriptions of organisms in both groups and recent documentations looking into the organisms' taxonomy and ecology [39,40]. Fluctuations of MPB populations are believed to be influenced by abiotic weather conditions.…”

Phytochemicals as mediators for host range expansion of a native invasive forest insect herbivore

“…Shortly after the invasion of lodgepole pine forests in Alberta in 2006–2007, beetles arrived in the hybrid zone and spent several generations there before flying into the more jack pine‐dominated forests in north‐eastern Alberta in 2011 (Lusebrink et al ., ). The invasion of this hybrid zone is likely a result of the rich phenotypic plasticity of, and adaptation to colonize many Pinus species with distinct chemical profiles by, MPB and its fungal symbionts within their historical range (Bentz et al ., ; Ojeda Alayon et al ., ). The chemical profile of the hybrids is intermediate between that of the two pine species (Table ).…”

“…In the current study, chemical similarity (or taxonomic relatedness) between the novel and historical hosts as well as compatibility of beetles with novel phytochemistry likely explain ‘colonization by ecological fitness’ of MPB in the novel pine habitats. Likewise, both MPB and its symbiotic fungi show large phenotypic variations in their historical range (Bentz et al ., ; Ojeda Alayon et al ., ), which have likely acted as a ‘stepping stone’ to colonize jack pine forests. Similarly, ecological fitting has been discussed to explain host switching of invasive emerald ash borer ( Agrilus planipennis ) in North America (Cipolini & Peterson, ).…”

Genome-wide signals of drift and local adaptation during rapid lineage divergence in a songbird

“…Importantly, GEA methods can correct for population history by controlling for general patterns of neutral genomic variation (Rellstab et al 2015; Forester et al 2016), allowing us to separate the respective effects of drift and selection in generating and maintaining variability. GEA analyses have greatly benefitted from the development of high-throughput sequencing techniques, resulting in a number of studies focusing on the genomic variability associated with environmental parameters in groups as diverse as plants (Lasky et al 2012; Jones et al 2013; De Kort et al 2014; Nadeau et al 2016; Sork et al 2016), fungus (Ojeda Alayon et al 2017), wolves (Forester et al 2017) and birds (Manthey and Moyle 2015; Safran et al 2016; Szulkin et al 2016; Termignoni-García et al 2017).…”