Polytene chromosomes as indicators of phylogeny in several species groups of Drosophila
© O'Grady et al; licensee BioMed Central Ltd. 2001
Received: 17 May 2001
Accepted: 10 October 2001
Published: 10 October 2001
Polytene chromosome banding patterns have long been used by Drosophila evolutionists to infer degree of relatedness among taxa. Recently, nucleotide sequences have preempted this traditional method. We place the classical Drosophila evolutionary biology tools of polytene chromosome inversion analysis in a phylogenetic context and assess their utility in comparison to nucleotide sequences.
A simultaneous analysis framework was used to examine the congruence of the chromosomal inversion data with more recent DNA sequence data in four Drosophila species groups – the melanogaster, virilis, repleta, and picture wing. Inversions and nucleotides were highly congruent with one another based on incongruence length difference and partitioned Bremer support values. Inversion phylogenies were less resolved because of fewer numbers of characters. Partitioned Bremer supports, corrected for the number of characters in each matrix, were higher for inversion matrices.
Polytene chromosome data are highly congruent with DNA sequence data and, when placed in a simultaneous analysis framework, are shown to be more information rich than nucleotide data.
Species in the family Drosophilidae have been premier research subjects in evolutionary biology since T. H. Morgan first used Drosophila melanogaster as a genetic tool in the early part of the 20th Century. Polytene chromosome phylogenies have become commonplace in the examination of this family of flies. The chromosomal analyses have been used in two ways in evolutionary studies. The first use is as genetic markers [1, 2] in which the chromosomal inversions are considered alleles and are utilized to examine gene flow and other population genetic parameters. The second use of polytene chromosomes in evolutionary studies is as tracers of phylogeny [3–7]. This approach has resulted in important and detailed chromosomal phylogenies for several groups of flies in the genus Drosophila. Lists of species for which polytene chromosome maps have been produced are available [8, 9], and over 300 species of Drosophila have been examined at this level. In particular, extensive chromosomal phylogenies for flies in the picture wing,melanogaster, virilis, and repleta species groups exist. Cladistic analyses of the chromosomal data for these groups exist for the picture wing and melanogaster species groups . More recently, large amounts of DNA sequence information have been collected for these and many other species groups, yet no detailed analysis of the overall utility of chromosomal inversion data or of their congruence with DNA sequence data has been carried out.
The main objective of the present study is to place the chromosomal inversion data into a phylogenetic framework. We examine the congruence of DNA sequence characters and chromosomal inversion data in four different species groups in the genus Drosophila (picture wing, repleta, melanogaster and virilis) to assess the relative contribution to phylogenetic hypotheses that the two different sources of character information make.
Results and Discussion
Data Sources for the five data matrices used in this study.
Tree statistics for the four analyses.
picture wing group
Results of partitioning Bremer support to molecular and inversion character sources.
corrected total BS
% zero or
Classical Drosophila studies have used chromosomal inversions to understand phylogeny and speciation. More recent DNA sequence information can be combined with these classical data to make inferences about phylogeny and species divergence. The approach we have taken here is to combine the chromosomal inversion data with DNA sequence data to examine some of the classical notions of Drosophila evolution. Our results suggest that there is a great deal of congruence among DNA sequence data and chromosomal inversion data. Although this result is reassuring, there are still some areas of the phylogenies of the four species groups examined here that are not congruent. These areas are indicative of poor phylogenetic signal from one or both of the kinds of data – DNA and chromosomal inversion data. Chromosomal inversion data are much more information rich as assessed in the present study, and this is probably due to the higher consistency of these characters. This higher consistency stems from that fact that, while nucleotide characters have only four possible states to change to and from, chromosome breaks can occur at many different locations. Therefore, it is much simpler to change from an A to a T in two unrelated lineages than it is to have the exact same chromosome break in those same lineages.
Materials and Methods
Four data matrices were constructed using DNA sequences and chromosomal inversion data from the literature (Table 1). The four species groups for which we have obtained inversion data represent the four major species groups for which such data exist. Chromosome inversion information for other smaller groups such as the antopocerus species group (Hawaiian Drosophila) is published , however DNA sequence data are not yet available for these groups.
Phylogenetic trees were generated using PAUP 4.0b7 . In order to assess the relative contribution of chromosomal inversion and DNA sequence data we placed our analysis in a simultaneous analysis framework [15–17]. Bootstrap values were computed using PAUP 4.0b7. Decay indices were computed using AUTODECAY  and using the methods described in Baker et al. . Significance of Incongruence Length Differences (ILDs [20, 21]) were calculated using the Partition Homogeneity Option in PAUP 4.0b7 . Partitioned Bremer supports for the inversion partition and the DNA partition were calculated using the approaches outlined in Baker et al. .
Here we include definitions of several phylogenetic measures used in this paper. The consistency index (CI; ) is used to determine how much homoplasy (i.e., how many times a character evolves on a tree) a given character displays. The CI of a character is the mimimum number of steps for that character on a given tree divided by the total number of steps reconstructed for that character on the same tree. Those characters which are highly consistent, or without homoplasy, would have a consistency index of 1.
The decay index or Bremer support value is used to measure support at a node of interest in a phylogenetic tree. To obtain the decay index, the treelength of a tree constrained not to contain a node of interest is substracted from the unconstrained (most parsimonious) treelength. Higher numbers generally indicate greater support at a node. Partitioned Bremer support (PBS; ) measures the amount of support provided by each individual partition to the DI for every node in the combined analysis phylogenies. PBS is an extension of the decay index in that it shows the contribution of each partition to the decay index of every node on the combined analysis tree. To obtain the PBS value for a given node on a combined tree, the length of the partition on the unconstrained combined tree is subtracted from the length of a partition on a tree constrained to not contain the node of interest. If the partition supports a relationship represented by a node in the combined tree, then the PBS value will be positive. If, on the other hand, a partition supports an alternative relationship, the PBS value will be negative. The magnitude of PBS values indicate the level of support for, or disagreement with, a node. The sum of all partition lengths for any given node will always equal the decay index for that node on the total evidence tree.
- Powell JR: Progress and Prospects in Evolutionary Biology:. The Drosophila Model. Oxford, Oxford University Press,. 1997Google Scholar
- Krimbas CB, Powell JR: Drosophila Inversion Polymorphism. Boca Raton, CRC Press,. 1992Google Scholar
- Carson HL: Chromosomal tracers of evolution. Science. 1970, 168: 1414-1418.View ArticlePubMedGoogle Scholar
- Carson HL: Tracing ancestry with chromosomal sequences. TREE. 1987, 2: 203-207. 10.1016/0169-5347(87)90021-8.PubMedGoogle Scholar
- Lemunier F, David JR, Tsacas L: The melanogaster species group. In: The Genetics and Biology of Drosophila Vol 3e (Edited by Ashburner, M, Carson, H. L., Thompson, J. N) New York, Academic Press,. 1986, 148-256.Google Scholar
- Throckmorton LH: The virilis species group. In: The Genetics and Biology of Drosophila Vol 3b (Edited by Ashburner, M, Carson, H. L., Thompson, J. N) New York, Academic Press,. 1982, 227-296.Google Scholar
- Wasserman M: Cytological evolution of the Drosophila repleta group. Drosophila Inversion Polymorphism. Edited by: Krimbas, C. B., Powell, J. R. 1992, Boca Raton, CRC Press, 455-552.Google Scholar
- Ashburner M: Drosophila : A Laboratory Handbook. New York, Cold Spring Harbor Press,. 1989Google Scholar
- Ashburner M, Carson HL: A checklist of maps of polytene chromosomes of drosophilids. Dros. Inf. Serv. 1983, 59: 148-151.Google Scholar
- Kaneshiro KY, Gillespie R, Carson HL: Chromosomes and male genitalia of Hawaiian Drosophila : tools for interpreting phylogeny and geography. In: Hawaiian Biogeography: Evolution on a Hotspot Archipelago (Edited by, Wagner, W.L., Funk, V. A.) Washington, DC, Smithsonian Institution Press,. 1995, 52-72.Google Scholar
- Lemunier F, Ashburner M: Relationships in the melanogaster species subgroup of the genus Drosophila (Sophophora). II. Phylogenetic relationships of six species based upon polytene banding sequences. Proc. R. Soc. Lond. B. 1976, 193: 257-294.Google Scholar
- Sanderson M, Donoghue M: Patterns of variation in levels of homoplasy. Evolution. 1992, 43: 1781-1795.View ArticleGoogle Scholar
- Yoon JS, Richardson R: Evolution of the Hawaiian Drosophilidae II. Patterns and rates of chromosome evolution in the Antopocerus phylogeny. Genetics. 1976, 83: 827-843.PubMed CentralPubMedGoogle Scholar
- Swofford D: PAUP*: Phylogenetic Analysis Using Parsimony* (and other methods), 4.0b7 beta version. Sunderland, MA, Sinauer Associates,. 2001Google Scholar
- Nixon K, Carpenter J: On simultaneous analysis. Cladistics. 1996, 12: 221-241. 10.1006/clad.1996.0016.View ArticleGoogle Scholar
- Kluge A: A concern for evidence and a phylogenetic hypothesis of relationships among Epicrates (Boidae, Serpentes). Syst. Zool. 1989, 38: 7-25.View ArticleGoogle Scholar
- Brower AVZ, DeSalle R, Vogler AP: Gene trees, species trees, and systematics: a cladistic perspective. Annu. Rev. Ecol. Syst. 1996, 27: 423-450. 10.1146/annurev.ecolsys.27.1.423.View ArticleGoogle Scholar
- Eriksson T: Auto-Decay. Software and documentation, version 2.9.5. Department of Botany, Stockholm University,. 1996Google Scholar
- Baker RH, Yu X, DeSalle R: Assessing the relative contribution of molecular and morphological characters in simultaneous analysis trees. Mol. Phyl. Evol. 1998, 9: 427-436. 10.1006/mpev.1998.0519.View ArticleGoogle Scholar
- Farris JS, Kallersjo M, Kluge AG, Bult C: Testing significance of congruence. Cladistics. 1994, 10: 315-320. 10.1006/clad.1994.1021.View ArticleGoogle Scholar
- Farris JS, Kallersjo M, Kluge AG, Bult C: Constructing a significance test for incongruence. Syst. Biol. 1995, 44: 570-572.View ArticleGoogle Scholar
- Kambysellis MP, Ho KF, Craddock EM, Piano F, Parisi M, Cohen J: Patterns of ecological shifts in the diversification of Hawaiian Drosophila inferred from a molecular phylogeny. Current Biology. 1995, 5: 1129-1139.View ArticlePubMedGoogle Scholar
- Coyne JA, Kreitman M: Evolutionary genetics of two sibling species, Drosophila simulans and D. sechellia. Evolution. 1986, 40: 673-691.View ArticleGoogle Scholar
- Cohn VH, Moore GP: Organization and evolution of the alcohol dehydrogenase gene in Drosophila. Mol. Biol. Evol. 1988, 5: 154-166.PubMedGoogle Scholar
- Ashburner M: Genbank accession number X54118. 1990Google Scholar
- Moses K, Heberlein U, Ashburner M: The Adh gene promoters of Drosophila melanogaster and Drosophila orena are functionally conserved and share features of sequence structure and nuclease-protected sites. Mol. Cell. Biol. 1990, 10: 539-548.PubMed CentralView ArticlePubMedGoogle Scholar
- McDonald JH, Kreitman M: Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991, 351: 652-654. 10.1038/351652a0.View ArticlePubMedGoogle Scholar
- Jeffs PS, Holmes EC, Ashburner M: The molecular evolution of the alcohol dehydrogenase and alcohol dehydrogenase-related genes in the Drosophila melanogaster species subgroup. Mol. Biol. Evol. 1994, 11: 287-304.PubMedGoogle Scholar
- Caccone A, Moriyama EN, Gleason JM, Nigro L, Powell JR: A molecular phylogeny for the Drosophila melanogaster subgroup and the problem of polymorphism data. Mol. Biol. Evol. 1996, 13: 1224-1232.View ArticlePubMedGoogle Scholar
- Ruiz Linares A, Hancock JM, Dover GA: Secondary structure constraints on the evolution of Drosophila 28S ribosomal RNA expansion segments. J. Mol. Biol. 1991, 219: 381-390.View ArticlePubMedGoogle Scholar
- Pelandakis M, Solignac M: Molecular phylogeny of Drosophila based on ribosomal RNA sequences. J. Mol. Evol. 1993, 37: 525-543.View ArticlePubMedGoogle Scholar
- Samson ML, Wegnez M: The 5S ribosomal genes in the Drosophila melanogaster species subgroup: nucleotide sequence of a 5S unit from Drosophila simulans and Drosophila teissieri. Nucleic Acids Res. 1984, 12: 1003-1014.PubMed CentralView ArticlePubMedGoogle Scholar
- Paques F, Samson ML, Jordan P, Wegnez M: Structural evolution of the Drosophila 5S ribosomal genes. J. Mol. Evol. 1995, 41: 615-21.View ArticlePubMedGoogle Scholar
- Shibata H, Yamazaki T: Molecular evolution of the duplicated Amy locus in the Drosophila melanogaster species subgroup: concerted evolution only in the coding region and an excess of nonsynonymous substitutions in speciation. Genetics. 1995, 141: 223-236.PubMed CentralPubMedGoogle Scholar
- Tominaga H, Narise S: Sequence evolution of the Gpdh gene in the Drosophila virilis species group. Genetica. 1995, 96: 293-302.View ArticlePubMedGoogle Scholar
- Kitagawa H: Genbank accession numbers AB019507 AB019546-AB019550,. 1998Google Scholar
- Nurminsky DI, Moriyama EN, Lozovskaya ER, Hartl DL: Molecular phylogeny and genome evolution in the Drosophila virilis species group duplications of the alcohol dehydrogenase gene. Mol. Biol. Evol. 1996, 13: 132-149.View ArticlePubMedGoogle Scholar
- Durando CM, Baker RH, Etges WJ, Heed WB, Wasserman M, DeSalle R: Phylogenetic analysis of the repleta species group of the genus Drosophila using multiple sources of characters. Mol. Phyl. Evol. 2000, 16: 296-307. 10.1006/mpev.2000.0824.View ArticleGoogle Scholar
- Kulge AG, Farris JS: Quantitative phyletics and the phylogeny of the anurans. Syst. Zool. 1969, 18: 1-32.View ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article: verbatim copying and redistribution of this article are permitted in all media for any purpose, provided this notice is preserved along with the article's original URL.