Chromosomal Translocations in Black Flies (Diptera: Simuliidae)—Facilitators of Adaptive Radiation?

Abstract

A macrogenomic investigation of a Holarctic clade of black flies—the Simulium cholodkovskii lineage—provided a platform to explore the implications of a unique, synapomorphic whole-arm interchange in the evolution of black flies. Nearly 60 structural rearrangements were discovered in the polytene complement of the lineage, including 15 common to all 138 analyzed individuals, relative to the central sequence for the entire subgenus Simulium. Three species were represented, of which two Palearctic entities (Simulium cholodkovskii and S. decimatum) were sympatric; an absence of hybrids confirmed their reproductive isolation. A third (Nearctic) entity had nonhomologous sex chromosomes, relative to the other species, and is considered a separate species, for which the name Simulium nigricoxum is revalidated. A cytophylogeny is inferred and indicates that the two Palearctic taxa are sister species and these, in turn, are the sister group of the Nearctic species. The rise of the S. cholodkovskii lineage encompassed complex chromosomal and genomic restructuring phenomena associated with speciation in black flies, viz. expression of one and the same rearrangement as polymorphic, fixed, or sex linked in different species; taxon-specific differentiation of sex chromosomes; and reciprocal translocation of chromosome arms. The translocation is hypothesized to have occurred early in male spermatogonia, with the translocated chromosomal complement being transmitted to the X- and Y-bearing sperm during spermatogenesis, resulting in alternate disjunction of viable F1 translocation heterozygotes and the eventual formation of more viable and selectable F2 translocation homozygous progeny. Of 11 or 12 independently derived whole-arm interchanges known in the family Simuliidae, at least six are associated with subsequent speciation events, suggesting a facilitating role of translocations in adaptive radiations. The findings are discussed in the context of potential structural and functional interactions for future genomic research.

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

“…rufibasis sensu stricto (= ‘A’), only in its putative sex chromosomes and autosomal polymorphisms. ‘B’ might be merely an example of sex-chromosome polymorphism, which is common in the Simuliidae [ 11 ], but we treat it here as a cytoform in recognition of the asserted role that sex chromosomes play in speciation of Diptera [ 35 ], including the Simuliidae [ 36 , 37 ]. To provide a taxonomic anchor, we provisionally regard ‘A’ as conspecific with chromosomally unstudied topotypical material of S .…”

“…Speciation in the Simuliidae has been associated with chromosomal phenomena, particularly coadaptation of sex chromosomes [ 37 ], cooption of individual rearrangements for different roles (e.g., fixation, X linkage) in different lineages, and more rarely, larger genomic restructuring events such as translocations [ 36 ]. Of the 15 Vietnamese cytoforms, four or fewer ( S .…”

River-specific macrogenomic diversity in Simulium guianense s. l. (Diptera: Simuliidae), a complex of tropical American vectors associated with human onchocerciasis

“…If the inversions reflect common ancestry, as we suggest, they exhibit the typical pattern in the Simuliidae: the ability of a single inversion to assume different states (e.g., fixation, loss, or polymorphism) in separate evolutionary lineages [29,39,43,44]. …”

The Evolution of Insect Metallothioneins

“…The high rate of chromosomal rearrangement in the Diptera (Ranz et al 2001;Adler et al 2016;Artemov et al 2017;Stewart and Rogers 2019) might explain the breakdown of the ancestral MT locus in the Diptera. In particular, the genomic locus surrounding MtnF is deeply rearranged in D. buzzatii (Calvete et al 2012).…”