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

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 co...

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Main Authors: Peter H Adler, Oyunchuluun Yadamsuren, William S Procunier
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2016-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC4922673?pdf=render
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author Peter H Adler
Oyunchuluun Yadamsuren
William S Procunier
author_facet Peter H Adler
Oyunchuluun Yadamsuren
William S Procunier
author_sort Peter H Adler
collection DOAJ
description 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.
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spelling doaj.art-23ba6f8bd110485d807cfeb43d35a6962022-12-22T01:50:47ZengPublic Library of Science (PLoS)PLoS ONE1932-62032016-01-01116e015827210.1371/journal.pone.0158272Chromosomal Translocations in Black Flies (Diptera: Simuliidae)-Facilitators of Adaptive Radiation?Peter H AdlerOyunchuluun YadamsurenWilliam S ProcunierA 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.http://europepmc.org/articles/PMC4922673?pdf=render
spellingShingle Peter H Adler
Oyunchuluun Yadamsuren
William S Procunier
Chromosomal Translocations in Black Flies (Diptera: Simuliidae)-Facilitators of Adaptive Radiation?
PLoS ONE
title Chromosomal Translocations in Black Flies (Diptera: Simuliidae)-Facilitators of Adaptive Radiation?
title_full Chromosomal Translocations in Black Flies (Diptera: Simuliidae)-Facilitators of Adaptive Radiation?
title_fullStr Chromosomal Translocations in Black Flies (Diptera: Simuliidae)-Facilitators of Adaptive Radiation?
title_full_unstemmed Chromosomal Translocations in Black Flies (Diptera: Simuliidae)-Facilitators of Adaptive Radiation?
title_short Chromosomal Translocations in Black Flies (Diptera: Simuliidae)-Facilitators of Adaptive Radiation?
title_sort chromosomal translocations in black flies diptera simuliidae facilitators of adaptive radiation
url http://europepmc.org/articles/PMC4922673?pdf=render
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AT oyunchuluunyadamsuren chromosomaltranslocationsinblackfliesdipterasimuliidaefacilitatorsofadaptiveradiation
AT williamsprocunier chromosomaltranslocationsinblackfliesdipterasimuliidaefacilitatorsofadaptiveradiation