The X chromosome of the German cockroach, Blattella germanica, is homologous to a fly X chromosome despite 400 million years divergence

Abstract Background Sex chromosome evolution is a dynamic process that can proceed at varying rates across lineages. For example, different chromosomes can be sex-linked between closely related species, whereas other sex chromosomes have been conserved for > 100 million years. Cases of long-term...

Full description

Bibliographic Details
Main Authors: Richard P. Meisel, Pablo J. Delclos, Judith R. Wexler
Format: Article
Language:English
Published: BMC 2019-12-01
Series:BMC Biology
Subjects:
Online Access:https://doi.org/10.1186/s12915-019-0721-x
_version_ 1818352273223319552
author Richard P. Meisel
Pablo J. Delclos
Judith R. Wexler
author_facet Richard P. Meisel
Pablo J. Delclos
Judith R. Wexler
author_sort Richard P. Meisel
collection DOAJ
description Abstract Background Sex chromosome evolution is a dynamic process that can proceed at varying rates across lineages. For example, different chromosomes can be sex-linked between closely related species, whereas other sex chromosomes have been conserved for > 100 million years. Cases of long-term sex chromosome conservation could be informative of factors that constrain sex chromosome evolution. Cytological similarities between the X chromosomes of the German cockroach (Blattella germanica) and most flies suggest that they may be homologous—possibly representing an extreme case of long-term conservation. Results To test the hypothesis that the cockroach and fly X chromosomes are homologous, we analyzed whole-genome sequence data from cockroaches. We found evidence in both sequencing coverage and heterozygosity that a significant excess of the same genes are on both the cockroach and fly X chromosomes. We also present evidence that the candidate X-linked cockroach genes may be dosage compensated in hemizygous males. Consistent with this hypothesis, three regulators of transcription and chromatin on the fly X chromosome are conserved in the cockroach genome. Conclusions Our results support our hypothesis that the German cockroach shares the same X chromosome as most flies. This may represent the convergent evolution of the X chromosome in the lineages leading to cockroaches and flies. Alternatively, the common ancestor of most insects may have had an X chromosome that resembled the extant cockroach and fly X. Cockroaches and flies diverged ∼ 400 million years ago, which would be the longest documented conservation of a sex chromosome. Cockroaches and flies have different mechanisms of sex determination, raising the possibility that the X chromosome was conserved despite the evolution of the sex determination pathway.
first_indexed 2024-12-13T18:51:01Z
format Article
id doaj.art-761813e8649c44018733e4529824f621
institution Directory Open Access Journal
issn 1741-7007
language English
last_indexed 2024-12-13T18:51:01Z
publishDate 2019-12-01
publisher BMC
record_format Article
series BMC Biology
spelling doaj.art-761813e8649c44018733e4529824f6212022-12-21T23:34:56ZengBMCBMC Biology1741-70072019-12-0117111410.1186/s12915-019-0721-xThe X chromosome of the German cockroach, Blattella germanica, is homologous to a fly X chromosome despite 400 million years divergenceRichard P. Meisel0Pablo J. Delclos1Judith R. Wexler2Department of Biology and Biochemistry, University of HoustonDepartment of Biology and Biochemistry, University of HoustonDepartment of Ecology and Evolution, University of California, DavisAbstract Background Sex chromosome evolution is a dynamic process that can proceed at varying rates across lineages. For example, different chromosomes can be sex-linked between closely related species, whereas other sex chromosomes have been conserved for > 100 million years. Cases of long-term sex chromosome conservation could be informative of factors that constrain sex chromosome evolution. Cytological similarities between the X chromosomes of the German cockroach (Blattella germanica) and most flies suggest that they may be homologous—possibly representing an extreme case of long-term conservation. Results To test the hypothesis that the cockroach and fly X chromosomes are homologous, we analyzed whole-genome sequence data from cockroaches. We found evidence in both sequencing coverage and heterozygosity that a significant excess of the same genes are on both the cockroach and fly X chromosomes. We also present evidence that the candidate X-linked cockroach genes may be dosage compensated in hemizygous males. Consistent with this hypothesis, three regulators of transcription and chromatin on the fly X chromosome are conserved in the cockroach genome. Conclusions Our results support our hypothesis that the German cockroach shares the same X chromosome as most flies. This may represent the convergent evolution of the X chromosome in the lineages leading to cockroaches and flies. Alternatively, the common ancestor of most insects may have had an X chromosome that resembled the extant cockroach and fly X. Cockroaches and flies diverged ∼ 400 million years ago, which would be the longest documented conservation of a sex chromosome. Cockroaches and flies have different mechanisms of sex determination, raising the possibility that the X chromosome was conserved despite the evolution of the sex determination pathway.https://doi.org/10.1186/s12915-019-0721-xSex chromosomeEvolutionInsectArthropod genomicsDosage compensation
spellingShingle Richard P. Meisel
Pablo J. Delclos
Judith R. Wexler
The X chromosome of the German cockroach, Blattella germanica, is homologous to a fly X chromosome despite 400 million years divergence
BMC Biology
Sex chromosome
Evolution
Insect
Arthropod genomics
Dosage compensation
title The X chromosome of the German cockroach, Blattella germanica, is homologous to a fly X chromosome despite 400 million years divergence
title_full The X chromosome of the German cockroach, Blattella germanica, is homologous to a fly X chromosome despite 400 million years divergence
title_fullStr The X chromosome of the German cockroach, Blattella germanica, is homologous to a fly X chromosome despite 400 million years divergence
title_full_unstemmed The X chromosome of the German cockroach, Blattella germanica, is homologous to a fly X chromosome despite 400 million years divergence
title_short The X chromosome of the German cockroach, Blattella germanica, is homologous to a fly X chromosome despite 400 million years divergence
title_sort x chromosome of the german cockroach blattella germanica is homologous to a fly x chromosome despite 400 million years divergence
topic Sex chromosome
Evolution
Insect
Arthropod genomics
Dosage compensation
url https://doi.org/10.1186/s12915-019-0721-x
work_keys_str_mv AT richardpmeisel thexchromosomeofthegermancockroachblattellagermanicaishomologoustoaflyxchromosomedespite400millionyearsdivergence
AT pablojdelclos thexchromosomeofthegermancockroachblattellagermanicaishomologoustoaflyxchromosomedespite400millionyearsdivergence
AT judithrwexler thexchromosomeofthegermancockroachblattellagermanicaishomologoustoaflyxchromosomedespite400millionyearsdivergence
AT richardpmeisel xchromosomeofthegermancockroachblattellagermanicaishomologoustoaflyxchromosomedespite400millionyearsdivergence
AT pablojdelclos xchromosomeofthegermancockroachblattellagermanicaishomologoustoaflyxchromosomedespite400millionyearsdivergence
AT judithrwexler xchromosomeofthegermancockroachblattellagermanicaishomologoustoaflyxchromosomedespite400millionyearsdivergence