Contingency in the convergent evolution of a regulatory network: Dosage compensation in Drosophila.

The repeatability or predictability of evolution is a central question in evolutionary biology and most often addressed in experimental evolution studies. Here, we infer how genetically heterogeneous natural systems acquire the same molecular changes to address how genomic background affects adaptat...

Full description

Bibliographic Details
Main Authors: Christopher Ellison, Doris Bachtrog
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2019-02-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.3000094
_version_ 1819021060424597504
author Christopher Ellison
Doris Bachtrog
author_facet Christopher Ellison
Doris Bachtrog
author_sort Christopher Ellison
collection DOAJ
description The repeatability or predictability of evolution is a central question in evolutionary biology and most often addressed in experimental evolution studies. Here, we infer how genetically heterogeneous natural systems acquire the same molecular changes to address how genomic background affects adaptation in natural populations. In particular, we take advantage of independently formed neo-sex chromosomes in Drosophila species that have evolved dosage compensation by co-opting the dosage-compensation male-specific lethal (MSL) complex to study the mutational paths that have led to the acquisition of hundreds of novel binding sites for the MSL complex in different species. This complex recognizes a conserved 21-bp GA-rich sequence motif that is enriched on the X chromosome, and newly formed X chromosomes recruit the MSL complex by de novo acquisition of this binding motif. We identify recently formed sex chromosomes in the D. melanica and D. robusta species groups by genome sequencing and generate genomic occupancy maps of the MSL complex to infer the location of novel binding sites. We find that diverse mutational paths were utilized in each species to evolve hundreds of de novo binding motifs along the neo-X, including expansions of microsatellites and transposable element (TE) insertions. However, the propensity to utilize a particular mutational path differs between independently formed X chromosomes and appears to be contingent on genomic properties of that species, such as simple repeat or TE density. This establishes the "genomic environment" as an important determinant in predicting the outcome of evolutionary adaptations.
first_indexed 2024-12-21T04:01:06Z
format Article
id doaj.art-fe28cfbf6bc84b3694e66fdf10166ab1
institution Directory Open Access Journal
issn 1544-9173
1545-7885
language English
last_indexed 2024-12-21T04:01:06Z
publishDate 2019-02-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Biology
spelling doaj.art-fe28cfbf6bc84b3694e66fdf10166ab12022-12-21T19:16:43ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852019-02-01172e300009410.1371/journal.pbio.3000094Contingency in the convergent evolution of a regulatory network: Dosage compensation in Drosophila.Christopher EllisonDoris BachtrogThe repeatability or predictability of evolution is a central question in evolutionary biology and most often addressed in experimental evolution studies. Here, we infer how genetically heterogeneous natural systems acquire the same molecular changes to address how genomic background affects adaptation in natural populations. In particular, we take advantage of independently formed neo-sex chromosomes in Drosophila species that have evolved dosage compensation by co-opting the dosage-compensation male-specific lethal (MSL) complex to study the mutational paths that have led to the acquisition of hundreds of novel binding sites for the MSL complex in different species. This complex recognizes a conserved 21-bp GA-rich sequence motif that is enriched on the X chromosome, and newly formed X chromosomes recruit the MSL complex by de novo acquisition of this binding motif. We identify recently formed sex chromosomes in the D. melanica and D. robusta species groups by genome sequencing and generate genomic occupancy maps of the MSL complex to infer the location of novel binding sites. We find that diverse mutational paths were utilized in each species to evolve hundreds of de novo binding motifs along the neo-X, including expansions of microsatellites and transposable element (TE) insertions. However, the propensity to utilize a particular mutational path differs between independently formed X chromosomes and appears to be contingent on genomic properties of that species, such as simple repeat or TE density. This establishes the "genomic environment" as an important determinant in predicting the outcome of evolutionary adaptations.https://doi.org/10.1371/journal.pbio.3000094
spellingShingle Christopher Ellison
Doris Bachtrog
Contingency in the convergent evolution of a regulatory network: Dosage compensation in Drosophila.
PLoS Biology
title Contingency in the convergent evolution of a regulatory network: Dosage compensation in Drosophila.
title_full Contingency in the convergent evolution of a regulatory network: Dosage compensation in Drosophila.
title_fullStr Contingency in the convergent evolution of a regulatory network: Dosage compensation in Drosophila.
title_full_unstemmed Contingency in the convergent evolution of a regulatory network: Dosage compensation in Drosophila.
title_short Contingency in the convergent evolution of a regulatory network: Dosage compensation in Drosophila.
title_sort contingency in the convergent evolution of a regulatory network dosage compensation in drosophila
url https://doi.org/10.1371/journal.pbio.3000094
work_keys_str_mv AT christopherellison contingencyintheconvergentevolutionofaregulatorynetworkdosagecompensationindrosophila
AT dorisbachtrog contingencyintheconvergentevolutionofaregulatorynetworkdosagecompensationindrosophila