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.

Highlights

  • The role of translocations in genomic and karyotypic evolution of eukaryotes is apparent— from their involvement in speciation processes and their use as tools in experimental genetic breeding systems [1,2] to their causal molecular associations in human cancerous and noncancerous diseases [3,4]

  • Other examples include the adaptive radiation of mammalian species, such as mice, through Robertsonian fusions and whole-arm interchanges [6] and the discovery that complex structural rearrangements can occur in certain cancers defined as chromothripsis [7]

  • We present the discovery of a whole-arm interchange in two additional taxa related to Simulium nigricoxum, all three of which are members of the S. cholodkovskii lineage

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Summary

Introduction

The role of translocations in genomic and karyotypic evolution of eukaryotes is apparent— from their involvement in speciation processes and their use as tools in experimental genetic breeding systems [1,2] to their causal molecular associations in human cancerous and noncancerous diseases [3,4]. Other examples include the adaptive radiation of mammalian species, such as mice, through Robertsonian fusions and whole-arm interchanges [6] and the discovery that complex structural rearrangements can occur in certain cancers defined as chromothripsis [7]. We provide full resolution of the chromosomal banding patterns of these three taxa relative to the standard (central) banding sequence for the subgenus Simulium, interpret the taxonomic implications including a test of the species status of S. nigricoxum separate from S. decimatum, infer the phylogenetic relationships chromosomally, place the interchange discovery in the context of all known whole-arm interchanges in the Simuliidae, examine the association of whole-arm interchanges with adaptive radiations in the family, and comment on potential structural and functional interactions for future genomic research

Ethics Statement
July 2002
Results
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