Abstract
The European black fly Simulium (Simulium) colombaschense (Scopoli), once responsible for as many as 22,000 livestock deaths per year, is chromosomally mapped, permitting its evolutionary relationships and pest drivers to be inferred. The species is 12 fixed inversions removed from the standard sequence of the subgenus Simulium. Three of these fixed inversions, 38 autosomal polymorphisms, and a complex set of 12 X and 6 Y chromosomes in 29 zygotic combinations uniquely characterize S. colombaschense and reveal 5 cytoforms: ‘A’ in the Danube watershed, ‘B’ in Italy’s Adige River, ‘C’ in the Aliakmonas River of Greece, ‘D’ in the Aoös drainage in Greece, and ‘E’ in the Belá River of Slovakia. ‘C’ and ‘D’ are reproductively isolated from one another, and ‘B’ is considered a cytotype of ‘A,’ the probable name bearer of colombaschense. The species status of ‘E’ cannot be determined without additional collections. Three derived polytene sequences, based on outgroup comparisons, place S. colombaschense in a clade of species composed of the S. jenningsi, S. malyschevi, and S. reptans species groups. Only cytoforms ‘A’ and ‘B’ are pests. Within the Simuliidae, pest status is reached through one of two principal pathways, both of which promote the production of large populations of blood-seeking flies: (1) colonization of the world’s largest rivers (habitat specialization) or (2) colonization of multiple habitat types (habitat generalization). Evolutionary acquisition of the ability to colonize large rivers by an ancestor of the S. jenningsi-malyschevi-reptans clade set the scene for the pest status of S. colombaschense and other big-river members of the clade. In an ironic twist, the macrogenome of S. colombaschense reveals that the name associated with history’s worst simuliid pest represents a complex of species, two or more of which are nonpests potentially vulnerable to loss of their limited habitat.
Highlights
Pest status is not an inherent biological property, but rather the result of human interests conflicting with organismal traits
The advantages afforded by colonization of the largest rivers conspire to build pest populations that bankrupt the mind: 7 billion pupae of the North American cattle killer, S. vampirum, were estimated in one rocky weir across the North Saskatchewan River [71], and nearly 1 billion adults of S. jenningsi were estimated to emerge per km per day from large rivers in the eastern United States [62]
An understanding of the evolutionary factors that drive pest status can focus the search for genes responsible for the enabling traits
Summary
Pest status is not an inherent biological property, but rather the result of human interests conflicting with organismal traits. For black flies—among the most virulent pests of birds and mammals [2]—the extrinsic factors associated with pest status have been more accessible than the intrinsic, or genetic, factors. Extrinsic factors that promote pest problems of black flies include rainfall, which can increase available breeding areas, and habitat modifications (e.g., impoundment of rivers), which can increase freshwater productivity [3, 4]. Geographic variation in pest status, while initially inexplicable, can sometimes be explained by the presence of cryptic species that differ in blood hosts, breeding habitats, and other organismal properties [5]. Though largely a historical phenomenon, the greatest wholesale slaughter of domestic animals was caused by Simulium colombaschense (Scopoli), responsible in some years for more than 22,000 deaths along the Danube River of southeastern Europe [8]
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