Cryptic Biodiversity and the Origins of Pest Status Revealed in the Macrogenome of Simulium colombaschense (Diptera: Simuliidae), History’s Most Destructive Black Fly

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.

Vietnam, a Hotspot for Chromosomal Diversity and Cryptic Species in Black Flies (Diptera: Simuliidae)

“…We use the following previously applied [ 25 ] definition of cytoform: a chromosomally distinct entity recognizable at an individual or a population level, without regard to whether the entity is part of a larger breeding population (cytotype) or is reproductively isolated (cytospecies). New cytoforms of the S .…”

Rearrangement hotspots in the sex chromosome of the Palearctic black fly Simulium bergi (Diptera, Simuliidae)

“…Typically, however, the number of sex-linked rearrangements is more limited within a population, often to a single example, linked either to the X or the Y (Adler et al 2016). Yet, examples of multiple sex-linked rearrangements in a single population are not uncommon.…”

“…Yet, examples of multiple sex-linked rearrangements in a single population are not uncommon. Two cytoforms (‘A’ and ‘D’), probably cryptic species, of Simulium colombaschense (Scopoli, 1780), each exhibits sex-chromosome polymorphism within a population at one river site; ‘A’ has 4 X-linked and 1 Y-linked inversions at a single site, and ‘D’ has 4 X-linked and 4 Y-linked inversions (Adler et al 2016). Simulium conundrum Adler, Currie & Wood, 2004 (formerly Simulium tuberosum ‘FGH’) at a single site in Newfoundland has 4 Y-linked inversions but no X-linked inversions (McCreadie et al 1995).…”

“…For this comparison, we used the standard maps of Rothfels et al (1978) for the IS, IL, IIL, and IIIS arms and of Adler et al (2016) for the IIS and IIIL arms. Newly discovered inversions were numbered in order of discovery, following the last numbered inversion of Rothfels et al (1978) for IS and IIIL and of Huang et al (2011) for IIL.…”

The State of Phylogenetic Analysis: Narrow Visions and Simple Answers—Examples from the Diptera (flies)

“…If CO1 sequences were interpreted cladistically, there may be an interesting test of their reliability. In a few families of Diptera such as Simuliidae and Chironomidae, polytene chromosomes can be used to identify monophyletic groups, based on unique rearrangements that can be interpreted in some of these groups as synapomorphies (Adler et al, 2004;Adler et al, 2016aAdler et al, , 2016bSenatore et al, 2014). It would be informative to compare the two methods to determine the degree of congruence and especially so in a group that has been recognized on the basis of symplesiomorphy or includes an autapomorphic lineage (to see if the CO1 sequences can identify these).…”