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Genome-scale phylogeography resolves the native population structure of the Asian longhorned beetle, Anoplophora glabripennis (Motschulsky).

ABSTRACT: Human-assisted movement has allowed the Asian longhorned beetle (ALB, Anoplophora glabripennis (Motschulsky)) to spread beyond its native range and become a globally regulated invasive pest. Within its native range of China and the Korean peninsula, human-mediated dispersal has also caused cryptic translocation of insects, resulting in population structure complexity. Previous studies used genetic methods to detangle this complexity but were unable to clearly delimit native populations which is needed to develop downstream biosurveillance tools. We used genome-wide markers to define historical population structure in native ALB populations and contemporary movement between regions. We used genotyping-by-sequencing to generate 6102 single-nucleotide polymorphisms (SNPs) and amplicon sequencing to genotype 53 microsatellites. In total, we genotyped 712 individuals from ALB's native distribution. We observed six distinct population clusters among native ALB populations, with a clear delineation between northern and southern groups. Most of the individuals from South Korea were distinct from populations in China. Our results also indicate historical divergence among populations and suggest limited large-scale admixture, but we did identify a restricted number of cases of contemporary movement between regions. We identified SNPs under selection and describe a clinal allele frequency pattern in a missense variant associated with glycerol kinase, an important enzyme in the utilization of an insect cryoprotectant. We further demonstrate that small numbers of SNPs can assign individuals to geographic regions with high probability, paving the way for novel ALB biosurveillance tools.

SUBMITTER: Cui M

PROVIDER: S-EPMC9234632 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Wood is a highly intractable food source, yet many insects successfully colonize and thrive in this challenging niche. Overcoming the lignin barrier of wood is a key challenge in nutrient acquisition, but full depolymerization of intact lignin polymers has only been conclusively demonstrated in fungi and is not known to occur by enzymes produced by insects or bacteria. Previous research validated that lignocellulose and hemicellulose degradation occur within the gut of the wood boring insect, Anoplophora glabripennis (Asian longhorned beetle), and that a fungal species, Fusarium solani (ATCC MYA 4552), is consistently associated with the larval stage. While the nature of this relationship is unresolved, we sought to assess this fungal isolate's ability to degrade lignocellulose and cell wall polysaccharides and to extract nutrients from woody tissue. This gut-derived fungal isolate was inoculated onto a wood-based substrate and shotgun proteomics using Multidimensional Protein Identification Technology (MudPIT) was employed to identify 400 expressed proteins. Through this approach, we detected proteins responsible for plant cell wall polysaccharide degradation, including proteins belonging to 28 glycosyl hydrolase families and several cutinases, esterases, lipases, pectate lyases, and polysaccharide deacetylases. Proteinases with broad substrate specificities and ureases were observed, indicating that this isolate has the capability to digest plant cell wall proteins and recycle nitrogenous waste under periods of nutrient limitation. Additionally, several laccases, peroxidases, and enzymes involved in extracellular hydrogen peroxide production previously implicated in lignin depolymerization were detected. In vitro biochemical assays were conducted to corroborate MudPIT results and confirmed that cellulases, glycosyl hydrolases, xylanases, laccases, and Mn- independent peroxidases were active in culture; however, lignin- and Mn- dependent peroxidase activities were not detected While little is known about the role of filamentous fungi and their associations with insects, these findings suggest that this isolate has the endogenous potential to degrade lignocellulose and extract nutrients from woody tissue.

Project description:Culture-independent analysis of the gut of a wood-boring insect, Anoplophora glabripennis (Coleoptera: Cerambycidae), revealed a consistent association between members of the fungal Fusarium solani species complex and the larval stage of both colony-derived and wild A. glabripennis populations. Using the translation elongation factor 1-alpha region for culture-independent phylogenetic and operational taxonomic unit (OTU)-based analyses, only two OTUs were detected, suggesting that genetic variance at this locus was low among A. glabripennis-associated isolates. To better survey the genetic variation of F. solani associated with A. glabripennis, and establish its phylogenetic relationship with other members of the F. solani species complex, single spore isolates were created from different populations and multi-locus phylogenetic analysis was performed using a combination of the translation elongation factor alpha-1, internal transcribed spacer, and large subunit rDNA regions. These analyses revealed that colony-derived larvae reared in three different tree species or on artificial diet, as well as larvae from wild populations collected from three additional tree species in New York City and from a single tree species in Worcester, MA, consistently harbored F. solani within their guts. While there is some genetic variation in the F. solani carried between populations, within-population variation is low. We speculate that F. solani is able to fill a broad niche in the A. glabripennis gut, providing it with fungal lignocellulases to allow the larvae to grow and develop on woody tissue. However, it is likely that many F. solani genotypes could potentially fill this niche, so the relationship may not be limited to a single member of the F. solani species complex. While little is known about the role of filamentous fungi and their symbiotic associations with insects, this report suggests that larval A. glabripennis has developed an intimate relationship with F. solani that is not limited by geographic location or host tree.

Project description:The establishment of non-native species is commonly described as occurring in three phases: arrival, establishment, and dispersal. Both arrival and dispersal by the Asian longhorned beetle (Anoplophora glabripennis Motschulsky), a xylophagous Cerambycid native to China and the Korean peninsula, has been documented for multiple locations in both North America and Europe, however the transitional phase, establishment, is not well understood for this species due to the need to rapidly remove populations to prevent dispersal and assist eradication, and the evident variation in the behavior of populations. Here we describe the dynamics of an establishment event for the Asian longhorned beetle in a small, isolated population within the regulated quarantine zone near Worcester, Massachusetts, USA. These data were collected during an opportunity afforded by logistical limits on the Cooperative Asian Longhorned Beetle Eradication Program administered by state, federal, and local government partners. Seventy-one infested red maple (Acer rubrum) trees and 456 interspersed un-infested trees were surveyed in an isolated, recently established population within a ~0.29 ha stand in a suburban wetland conservation area in which nearly 90% of the trees were host species, and nearly 80% were Acer rubrum. Tree-ring analyses show that within this establishing population, Asian longhorned beetles initially infested one or two A. rubrum, before moving through the stand to infest additional A. rubrum based not on distance or direction, but on tree size, with infestation biased towards trees with larger trunk diameters. Survey data from the larger landscape suggest this population may have generated long-distance dispersers (~1400 m), and that these dispersal events occurred before the originally infested host trees were fully exploited by the beetle. The distribution and intensity of damage documented in this population suggest dispersal here may have been spatially more rapid and diffuse than in other documented infestations. Dispersal at these larger spatial scales also implies that when beetles move beyond the closed canopy of the stand, the direction of dispersal may be linked to prevailing winds.

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Genome-scale phylogeography resolves the native population structure of the Asian longhorned beetle, Anoplophora glabripennis (Motschulsky).

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