Comparative genomics of bdelloid rotifers: insights from desiccating and nondesiccating species
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Author(s)
Barraclough, TG
Nowell, Reuben
Wilson, Christopher
Smith, thomas
Type
Journal Article
Abstract
Bdelloid rotifers are a Class of
microscopic invertebrates that have existed for millions of years
apparently without sex or meiosis. They inhabit a variety of temporary and
permanent freshwater
habitats globally, and many species are remarkably tolerant of desiccation. Bdelloids offer an
opportunity to better understand the evolution of sex and recombination, but previous work has
emphasized desiccation as the cause of severa
l unusual genomic features in this group. Here, we
present high
-quality whole genome sequences of three bdelloid species:
Rotaria macrura
and
Rotaria
magnacalcarata,
which are both desiccation intolerant, and
Adineta ricciae
, which is desiccation
tolerant.
In combination with the published assembly of
Adineta vaga
, which is also desiccation tolerant, we apply a comparative genomics approach to evaluate the potential effects of desiccation
tolerance and asexuality on genome evolution in bdelloids. We find that ancestral tetraploidy is conserved among all four bdelloid species, but homologous divergence in obligately aquatic
Rotaria
genomes is unexpectedly low. This finding is contrary to current models regarding the role of desiccation in shaping bdelloid gen
omes. In addition, we find that homologous regions in
A. ricciae
are largely collinear and do not form palindromic repeats as observed in the published
A. vaga
assembly. Consequently, several features interpreted as genomic evidence for long
-term ameiotic
evolution are not general to all bdelloid species, even within the same genus. Finally, we substantiate previous
50
findings of high levels of horizontally transferred non
-metazoan genes in both desiccating and non
-
desiccating bdelloid species, and show that
this unusual feature is not shared by
other
animal phyla,
even those with desiccation
-tolerant representatives. These comparisons call into question the
proposed role of desiccation in mediating horizontal genetic transfer
microscopic invertebrates that have existed for millions of years
apparently without sex or meiosis. They inhabit a variety of temporary and
permanent freshwater
habitats globally, and many species are remarkably tolerant of desiccation. Bdelloids offer an
opportunity to better understand the evolution of sex and recombination, but previous work has
emphasized desiccation as the cause of severa
l unusual genomic features in this group. Here, we
present high
-quality whole genome sequences of three bdelloid species:
Rotaria macrura
and
Rotaria
magnacalcarata,
which are both desiccation intolerant, and
Adineta ricciae
, which is desiccation
tolerant.
In combination with the published assembly of
Adineta vaga
, which is also desiccation tolerant, we apply a comparative genomics approach to evaluate the potential effects of desiccation
tolerance and asexuality on genome evolution in bdelloids. We find that ancestral tetraploidy is conserved among all four bdelloid species, but homologous divergence in obligately aquatic
Rotaria
genomes is unexpectedly low. This finding is contrary to current models regarding the role of desiccation in shaping bdelloid gen
omes. In addition, we find that homologous regions in
A. ricciae
are largely collinear and do not form palindromic repeats as observed in the published
A. vaga
assembly. Consequently, several features interpreted as genomic evidence for long
-term ameiotic
evolution are not general to all bdelloid species, even within the same genus. Finally, we substantiate previous
50
findings of high levels of horizontally transferred non
-metazoan genes in both desiccating and non
-
desiccating bdelloid species, and show that
this unusual feature is not shared by
other
animal phyla,
even those with desiccation
-tolerant representatives. These comparisons call into question the
proposed role of desiccation in mediating horizontal genetic transfer
Date Issued
2018-04-24
Date Acceptance
2018-02-20
Citation
PLoS Biology, 2018, 16 (4)
ISSN
1544-9173
Publisher
Public Library of Science (PLoS)
Journal / Book Title
PLoS Biology
Volume
16
Issue
4
Copyright Statement
© 2018 Nowell et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Sponsor
Natural Environment Research Council (NERC)
Grant Number
NE/M01651X/1
Subjects
Science & Technology
Life Sciences & Biomedicine
Biochemistry & Molecular Biology
Biology
Life Sciences & Biomedicine - Other Topics
HORIZONTAL GENE-TRANSFER
COPY-NUMBER-VARIATION
TRANSPOSABLE ELEMENTS
DROSOPHILA-MELANOGASTER
ADINETA-RICCIAE
ACQUIRED GENES
CROSSING-OVER
MEIOTIC SEX
ANHYDROBIOTIC TARDIGRADES
DEGENERATE TETRAPLOIDY
06 Biological Sciences
11 Medical And Health Sciences
07 Agricultural And Veterinary Sciences
Developmental Biology
Publication Status
Published
Article Number
e2004830