Recent Strong Positive Selection on Drosophila melanogaster HDAC6, a Gene Encoding a Stress Surveillance Factor, as Revealed by Population Genomic Analysis

AbstractContrary to prevailing dogma, evolutionarily young and dynamic genes can encode essential functions. Here, we investigate genetic innovation in ZAD-ZNF genes, which encode the most abundant class of insect transcription factors. We find that evolutionarily dynamic ZAD-ZNF genes are more likely to encode essential functions in Drosophila melanogaster than ancient, conserved ZAD-ZNF genes. To understand the basis of this unexpected correlation, we focus on the Nicknack ZAD-ZNF gene. Nicknack is an evolutionarily young, poorly retained in Drosophila species, and evolves under strong positive selection, yet we find that it is necessary for larval development in D. melanogaster. We show that Nicknack encodes a heterochromatin-localizing protein like its closely related paralog Oddjob, also an evolutionarily dynamic, essential ZAD-ZNF gene. We find that the divergent D. simulans Nicknack protein can still localize to D. melanogaster heterochromatin and rescue viability of female but not male Nicknack-null D. melanogaster. Our findings suggest that innovation for rapidly changing heterochromatin functions might provide a general explanation for the essential functions of many evolutionarily dynamic ZAD-ZNF genes in insects.

Download Full-text

Innovation of heterochromatin functions drives rapid evolution of essential ZAD-ZNF genes in Drosophila

eLife ◽

10.7554/elife.63368 ◽

2020 ◽

Vol 9 ◽

Author(s):

Bhavatharini Kasinathan ◽

Serafin U Colmenares ◽

Hannah McConnell ◽

Janet M Young ◽

Gary H Karpen ◽

...

Keyword(s):

Drosophila Melanogaster ◽

Transcription Factors ◽

Positive Selection ◽

Larval Development ◽

Rapid Evolution ◽

Strong Positive Selection

Contrary to dogma, evolutionarily young and dynamic genes can encode essential functions. We find that evolutionarily dynamic ZAD-ZNF genes, which encode the most abundant class of insect transcription factors, are more likely to encode essential functions in Drosophila melanogaster than ancient, conserved ZAD-ZNF genes. We focus on the Nicknack ZAD-ZNF gene, which is evolutionarily young, poorly retained in Drosophila species, and evolves under strong positive selection. Yet we find that it is necessary for larval development in D. melanogaster. We show that Nicknack encodes a heterochromatin-localizing protein like its paralog Oddjob, also an evolutionarily dynamic yet essential ZAD-ZNF gene. We find that the divergent D. simulans Nicknack protein can still localize to D. melanogaster heterochromatin and rescue viability of female but not male Nicknack-null D. melanogaster. Our findings suggest that innovation for rapidly changing heterochromatin functions might generally explain the essentiality of many evolutionarily dynamic ZAD-ZNF genes in insects.

Download Full-text

Population Genomic Analysis of Base Composition Evolution in Drosophila melanogaster

Genome Biology and Evolution ◽

10.1093/gbe/evs097 ◽

2012 ◽

Vol 4 (12) ◽

pp. 1245-1255 ◽

Cited By ~ 13

Author(s):

Yu-Ping Poh ◽

Chau-Ti Ting ◽

Hua-Wen Fu ◽

Charles H. Langley ◽

David J. Begun

Keyword(s):

Drosophila Melanogaster ◽

Base Composition ◽

Genomic Analysis ◽

Population Genomic

Download Full-text

Population genomic analysis uncovers African and European admixture in Drosophila melanogaster populations from the southeastern United States and Caribbean Islands

10.1101/009092 ◽

2014 ◽

Author(s):

Joyce Y Kao ◽

Asif Zubair ◽

Matthew P Salomon ◽

Sergey V Nuzhdin ◽

Daniel Campo

Keyword(s):

United States ◽

Drosophila Melanogaster ◽

Population Structure ◽

North American ◽

East Coast ◽

Genomic Analysis ◽

European Ancestry ◽

Caribbean Islands ◽

Population Genomic ◽

Caribbean Populations

Genome sequences from North American Drosophila melanogaster populations have become available to the scientific community. Deciphering the underlying population structure of these resources is crucial to make the most of these population genomic resources. Accepted models of North American colonization generally purport that several hundred years ago, flies from Africa and Europe were transported to the east coast United States and the Caribbean Islands respectively and thus current east coast US and Caribbean populations are an admixture of African and European ancestry. Theses models have been constructed based on phenotypes and limited genetic data. In our study, we have sequenced individual whole genomes of flies from populations in the southeast US and Caribbean Islands and examined these populations in conjunction with population sequences from Winters, CA, (USA); Raleigh, NC (USA); Cameroon (Africa); and Montpellier (France) to uncover the underlying population structure of North American populations. We find that west coast US populations are most like European populations likely reflecting a rapid westward expansion upon first settlements into North America. We also find genomic evidence of African and European admixture in east coast US and Caribbean populations, with a clinal pattern of decreasing proportions of African ancestry with higher latitude further supporting the proposed demographic model of Caribbean flies being established by African ancestors. Our genomic analysis of Caribbean flies is the first study that exposes the source of previously reported novel African alleles found in east coast US populations.

Download Full-text

Molecular Evolution of Duplicated Amylase Gene Regions in Drosophila melanogaster: Evidence of Positive Selection in the Coding Regions and Selective Constraints in the cis-Regulatory Regions

Genetics ◽

10.1093/genetics/157.2.667 ◽

2001 ◽

Vol 157 (2) ◽

pp. 667-677

Author(s):

Hitoshi Araki ◽

Nobuyuki Inomata ◽

Tsuneyuki Yamazaki

Keyword(s):

Drosophila Melanogaster ◽

Molecular Evolution ◽

Positive Selection ◽

Natural Populations ◽

Sliding Window ◽

Selective Constraint ◽

Proximal Region ◽

Coding Regions ◽

Asian Populations ◽

Flanking Region

Abstract In this study, we randomly sampled Drosophila melanogaster from Japanese and Kenyan natural populations. We sequenced duplicated (proximal and distal) Amy gene regions to test whether the patterns of polymorphism were consistent with neutral molecular evolution. Fst between the two geographically distant populations, estimated from Amy gene regions, was 0.084, smaller than reported values for other loci, comparing African and Asian populations. Furthermore, little genetic differentiation was found at a microsatellite locus (DROYANETSB) in these samples (Gst′=−0.018). The results of several tests (Tajima's, Fu and Li's, and Wall's tests) were not significantly different from neutrality. However, a significantly higher level of fixed replacement substitutions was detected by a modified McDonald and Kreitman test for both populations. This indicates that positive selection occurred during or immediately after the speciation of D. melanogaster. Sliding-window analysis showed that the proximal region 1, a part of the proximal 5′ flanking region, was conserved between D. melanogaster and its sibling species, D. simulans. An HKA test was significant when the proximal region 1 was compared with the 5′ flanking region of Alcohol dehydrogenase (Adh), indicating a severe selective constraint on the Amy proximal region 1. These results suggest that natural selection has played an important role in the molecular evolution of Amy gene regions in D. melanogaster.

Download Full-text

cDNA cloning and chromosomal mapping of the gene encoding adenylate kinase 2 from Drosophila melanogaster

Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression ◽

10.1016/s0167-4781(99)00223-7 ◽

2000 ◽

Vol 1490 (1-2) ◽

pp. 109-114 ◽

Cited By ~ 3

Author(s):

Takafumi Noma ◽

Ryutaro Murakami ◽

Yasuhiro Yamashiro ◽

Koichi Fujisawa ◽

Sachie Inouye ◽

...

Keyword(s):

Drosophila Melanogaster ◽

Cdna Cloning ◽

Adenylate Kinase ◽

Chromosomal Mapping ◽

Gene Encoding

Download Full-text

Population Genomic Analysis of ALMS1 in Humans Reveals a Surprisingly Complex Evolutionary History

Molecular Biology and Evolution ◽

10.1093/molbev/msp045 ◽

2009 ◽

Vol 26 (6) ◽

pp. 1357-1367 ◽

Cited By ~ 18

Author(s):

Laura B. Scheinfeldt ◽

Shameek Biswas ◽

Jennifer Madeoy ◽

Caitlin F. Connelly ◽

Eric E. Schadt ◽

...

Keyword(s):

Evolutionary History ◽

Genomic Analysis ◽

Population Genomic ◽

Complex Evolutionary History

Download Full-text

Interacting proteins identified by genetic interactions: a missense mutation in alpha-tubulin fails to complement alleles of the testis-specific beta-tubulin gene of Drosophila melanogaster.

Molecular and Cellular Biology ◽

10.1128/mcb.9.3.875 ◽

1989 ◽

Vol 9 (3) ◽

pp. 875-884 ◽

Cited By ~ 24

Author(s):

T S Hays ◽

R Deuring ◽

B Robertson ◽

M Prout ◽

M T Fuller

Keyword(s):

Drosophila Melanogaster ◽

Missense Mutation ◽

Null Allele ◽

Genetic Interaction ◽

Structural Proteins ◽

Interacting Proteins ◽

Tubulin Gene ◽

Beta Tubulin ◽

Gene Encoding ◽

Alpha Tubulin

In this paper we demonstrate that failure to complement between mutations at separate loci can be used to identify genes that encode interacting structural proteins. A mutation (nc33) identified because it failed to complement mutant alleles of the gene encoding the testis-specific beta 2-tubulin of Drosophila melanogaster (B2t) did not map to the B2t locus. We show that this second-site noncomplementing mutation is a missense mutation in alpha-tubulin that results in substitution of methionine in place of valine at amino acid 177. Because alpha- and beta-tubulin form a heterodimer, our results suggest that the genetic interaction, failure to complement, is based on the structural interaction between the protein products of the two genes. Although the nc33 mutation failed to complement a null allele of B2t (B2tn), a deletion of the alpha-tubulin gene to which nc33 mapped complemented B2tn. Thus, the failure to complement appears to require the presence of the altered alpha-tubulin encoded by the nc33 allele, which may act as a structural poison when incorporated into either the tubulin heterodimer or microtubules.

Download Full-text