Diversity, migration routes, and worldwide population genetic structure of Lecanosticta acicola, the causal agent of brown spot needle blight

Abstract

Lecanosticta acicola is a pine needle pathogen causing brown spot needle blight that results in premature needle shedding with considerable damage described in North America, Europe, and Asia. Microsatellite and mating type markers were used to study the population genetics, migration history, and reproduction mode of the pathogen, based on a collection of 650 isolates from 27 countries and 26 hosts across the range of L. acicola. The presence of L. acicola in Georgia was confirmed in this study. Migration analyses indicate there have been several introduction events from North America into Europe. However, some of the source populations still appear to remain unknown. The populations in Croatia and western Asia appear to originate from genetically similar populations in North America. Intercontinental movement of the pathogen was reflected in an identical haplotype occurring on two continents, in North America (Canada) and Europe (Germany). Several shared haplotypes between European populations further suggests more local pathogen movement between countries. Moreover, migration analyses indicate that the populations in northern Europe originate from more established populations in central Europe. Overall, the highest genetic diversity was observed in south-eastern USA. In Europe, the highest diversity was observed in France, where the presence of both known pathogen lineages was recorded. Less than half of the observed populations contained mating types in equal proportions. Although there is evidence of some sexual reproduction taking place, the pathogen spreads predominantly asexually and through anthropogenic activity.

Keywords: Mycosphaerella dearnessii; Pinus; forest pathology; introduction pathways; invasive pathogen; mating type; microsatellites.

FIGURE 1

Map of the sampling locations (red dots) of Lecanosticta acicola. Yellow points indicate the weighted geographical midpoint of a particular sampling area and the representative population (Table S1). Definition of population codes: AUT, Austria; BLR, Belarus; CAN, Canada; CHE, Switzerland; CHN, China; COL, Colombia; CZE, Czech Republic; DEU, Germany; ESP, Spain; EST, Estonia; FRA, France; GEO, Georgia; HRV, Croatia; IRL, Ireland; ITA, Italy; JPN, Japan; LTU, Lithuania; LTV, Latvia; N‐USA, north‐eastern United States; MEX, Mexico; POL, Poland; PRT, Portugal; RUS, Russia; S‐USA, south‐eastern United States; SVK, Slovakia; SVN, Slovenia; SWE, Sweden; TUR, Turkey.

FIGURE 2

Principal coordinate analysis of Nei's genetic distance of 16 populations of Lecanosticta acicola. Definition of population codes: AUT, Austria; CAN, Canada; CHE, Switzerland; CZE, Czech Republic; DEU, Germany; ESP, Spain; EST, Estonia; FRA, France; HRV, Croatia; LTU, Lithuania; N‐USA, north‐eastern United States; POL, Poland; RUS, Russia; S‐USA, south‐eastern United States; SVN, Slovenia; TUR, Turkey.

FIGURE 3

Results of the Mantel test on geographical and Nei's genetic distances of populations with at least six samples (N [cc] ≥ 6). Each point represents the combination of geographical and genetic distance values for each pair of populations compared. Legend (bottom right corner) explains symbols and colours representing the population pairs on the figures. (a) All 16 populations from North America and Europe (including western Asia). (b) Thirteen populations from Europe (including western Asia). (c) Three populations from North America.

FIGURE 4

STRUCTURE clustering of the Lecanosticta acicola clone‐corrected dataset, representing K = 2–7. Optimal number of clusters (K = 2) by ΔK and (K = 7) by ln(Pr(X|K)). Population codes are displayed under the figure; above the figure division into regions as analysed in the migration analyses is displayed. Definition of population codes: AUT, Austria; BLR, Belarus; CAN, Canada; CHE, Switzerland; CHN, China; COL, Colombia; CZE, Czech Republic; DEU, Germany; ESP, Spain; EST, Estonia; FRA, France; GEO, Georgia; HRV, Croatia; IRL, Ireland; ITA, Italy; JPN, Japan; LTU, Lithuania; LTV, Latvia; N‐USA, north‐eastern United States; MEX, Mexico; POL, Poland; PRT, Portugal; RUS, Russia; S‐USA, south‐eastern United States; SVK, Slovakia; SVN, Slovenia; SWE, Sweden; TUR, Turkey.

FIGURE 5

The proportion of STRUCTURE clusters (K = 7) in Lecanosticta acicola populations with at least six samples (N [cc] ≥ 6). Definition of population codes: AUT, Austria; CAN, Canada; CHE, Switzerland; CZE, Czech Republic; DEU, Germany; ESP, Spain; EST, Estonia; FRA, France; HRV, Croatia; LTU, Lithuania; N‐USA, north‐eastern United States; POL, Poland; RUS, Russia; S‐USA, south‐eastern United States; SVN, Slovenia; TUR, Turkey.

FIGURE 6

Neighbour‐joining tree of genetic distances (Da, Nei, 1972) for 28 populations as implemented in POPTREE v. 2 with 10,000 bootstraps used to generate confidence at branch points. Definition of population codes: AUT, Austria; BLR, Belarus; CAN, Canada; CHE, Switzerland; CHN, China; COL, Colombia; CZE, Czech Republic; DEU, Germany; ESP, Spain; EST, Estonia; FRA, France; GEO, Georgia; HRV, Croatia; IRL, Ireland; ITA, Italy; JPN, Japan; LTU, Lithuania; LTV, Latvia; N‐USA, north‐eastern United States; MEX, Mexico; POL, Poland; PRT, Portugal; RUS, Russia; S‐USA, south‐eastern United States; SVK, Slovakia; SVN, Slovenia; SWE, Sweden; TUR, Turkey.

FIGURE 7

A graphical representation of the historical scenarios, most supported by the approximate Bayesian computation (ABC) analyses. A, ancestral population; U, unsampled population; N‐AME, north‐eastern America (N‐USA + CAN); S‐USA, south‐eastern United States; SW‐EUR, south‐western Europe; EUR, combined population of C‐EUR, HRV, and W‐ASIA; C‐EUR, central Europe; N‐EUR, northern Europe; HRV, Croatia; W‐ASIA, western Asia; b, bottleneck event; r1, r2, and r3, rates of admixture; thickness of line indicates the contribution from populations (r and r − 1).