Hemiplasy and homoplasy in the karyotypic phylogenies of mammals - PubMed (original) (raw)
Hemiplasy and homoplasy in the karyotypic phylogenies of mammals
Terence J Robinson et al. Proc Natl Acad Sci U S A. 2008.
Abstract
Phylogenetic reconstructions are often plagued by difficulties in distinguishing phylogenetic signal (due to shared ancestry) from phylogenetic noise or homoplasy (due to character-state convergences or reversals). We use a new interpretive hypothesis, termed hemiplasy, to show how random lineage sorting might account for specific instances of seeming "phylogenetic discordance" among different chromosomal traits, or between karyotypic features and probable species phylogenies. We posit that hemiplasy is generally less likely for underdominant chromosomal polymorphisms (i.e., those with heterozygous disadvantage) than for neutral polymorphisms or especially for overdominant rearrangements (which should tend to be longer-lived), and we illustrate this concept by using examples from chiropterans and afrotherians. Chromosomal states are especially powerful in phylogenetic reconstructions because they offer strong signatures of common ancestry, but their evolutionary interpretations remain fully subject to the principles of cladistics and the potential complications of hemiplasy.
Conflict of interest statement
The authors declare no conflict of interest.
Figures
Fig. 1.
Schematic representations of hemiplasy. Shown are the distributions of a genic or chromosomal polymorphism (Upper) and a set of genealogical lineages (Lower) that traversed successive speciation nodes in an organismal phylogeny (broad branches) only to become fixed, by lineage sorting, in descendant species in a pattern that appears at face value to be discordant with the species phylogeny. In these diagrams, species II and III both have the homologous and derived character “b,” so the gene tree gives the impression that species II and III are the more closely related. However, in truth species I and II are sister taxa, despite the fact that species I alone retains the ancestral genetic condition “a.”
Fig. 2.
Phylogenetic relationships among bat species representing four taxonomic families (redrawn from ref. 27). Also shown is the presence of the chromosomal synteny 1/6/5, which formerly was interpreted to be homoplasic (27) but might instead be an example of hemiplasy.
Fig. 3.
Competing phylogenetic hypotheses for species comprising the Afroinsectiphillia clade (aardvark, elephant shrew, golden mole, and tenrec). (A) Clade comprising the elephant shrew, tenrec, and golden mole to the exclusion of aardvark based on concatenations of nuclear and mitochondrial DNA sequences (40, 42). (B) Clade composed of aardvark plus tenrec and a weaker grouping of these taxa and the golden mole to the exclusion of elephant shrew based on a different concatenation (41). (C) Clade composed of aardvark and elephant shrew to the exclusion of golden mole based on cross-species CP (43).
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References
- Hennig W. Grundzüge einer Theorie der Phylogenetischen Systematik. Berlin: Deutscher Zentralverlag; 1950. (1996 Phylogenetic Systematics (University of Illinois Press, Urbana, Illinois) (English)
- Ferguson-Smith MA, Trifonov V. Mammalian karyotype evolution. Nat Rev Genet. 2007;8:950–962. - PubMed
- Avise JC, Robinson TJ. Hemiplasy: A new term in the lexicon of phylogenetics. Syst Biol. 2008;57:503–507. - PubMed
- Nei M. Molecular Evolutionary Genetics. New York: Columbia Univ Press; 1987.
- Rosenberg NA. The probability of topological concordance of gene trees and species trees. Theor Pop Biol. 2002;61:225–247. - PubMed