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A Comparative Summary of Genetic Distances in the Vertebrates from the Mitochondrial Cytochrome B Gene

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A Comparative Summary of Genetic Distances in the Vertebrates from the Mitochondrial Cytochrome B Gene A Comparative Summary of Genetic Distances in the Vertebrates from the Mitochondrial Cytochrome b Gene Glenn C. Johns1 and John C. Avise Department of Genetics, University of Georgia Mitochondrial cytochrome b (cytb) is among the most extensively sequenced genes to date across the vertebrates. Here, we employ nearly 2,000 cytb gene sequences from GenBank to calculate and compare levels of genetic distance between sister species, congeneric species, and confamilial genera within and across the major vertebrate taxonomic classes. The results of these analyses parallel and reinforce some of the principal trends in genetic distance estimates previously reported in a summary of the multilocus allozyme literature. In particular, surveyed avian taxa on average show signi®cantly less genetic divergence than do same-rank taxa surveyed in other vertebrate groups, notably amphibians and reptiles. Various biological possibilities and taxonomic ``artifacts'' are considered that might account for this pattern. Regardless of the explanation, by the yardstick of genetic divergence in this mtDNA gene, as well as genetic distances in allozymes, there is rather poor equivalency of taxonomic rank across some of the vertebrates. Introduction In 1982, Avise and Aquadro summarized the mul- quences of a single cytoplasmic gene vis-aÁ-vis those tilocus allozyme literature on mean genetic distances from protein-level assays of multiple nuclear loci. (D's) between congeneric species and confamilial genera The comparative perspectives adopted in this paper across the major vertebrate classes. Some salient trends differ somewhat from the usual immediate aim of most emerged. Notably, mean D values among avian conge- systematic studies, which is to reconstruct phylogenetic ners were typically lower than those for other vertebrate relationships within a taxonomic group. Rather than fo- groups. Congeneric species of amphibians and reptiles cusing here on the cladistic relationships of particular often tended toward the high end of the mean genetic taxa, we address questions of the following relational distance scale, whereas congeneric ®shes and mammals sort: Are the various taxonomic ranks in existing ver- generally were intermediate in magnitude of interspe- tebrate classi®cations equivalent with respect to genetic ci®c D's. Similar trends toward smaller genetic distances distance? In other words, by this standard, is a genus or for birds than for other vertebrate groups also pertained family of birds, for example, equivalent to its hierar- to comparisons of confamilial genera. chical counterpart in mammals or in amphibians? Here, we revisit the comparative approaches of Av- If the answer to the second question is ``no,'' pos- ise and Aquadro (1982) with another potential common sible explanations might include any one or a combi- yardstick: genetic differences in nucleotide sequence (p) nation of the following: (1) identical taxonomic ranks in of the mitochondrial cytochrome b (cytb) gene. Several different vertebrate groups differ by age; (2) they are of same age but differ in rate of molecular evolution; (3) rationales exist for summarizing the cytb literature. First, taxonomists working on some vertebrates tend to be cytb is the gene that is perhaps most extensively se- splitters, whereas others are lumpers; or (4) relevant bi- quenced to date for the vertebrates (Irwin, Kocher, and ological differences exist among vertebrate classes, such Wilson 1991; Lydeard and Roe 1997; Moore and De- as in rates of morphological evolution. Such possibilities Filippis 1997). Second, the evolutionary dynamics of will be considered to explain the relatively small genetic the cytb gene and the biochemistry of the protein prod- distances that we summarize here for avian taxa. uct are better characterized than most other molecular systems (Esposti et al. 1993). Third, levels of genetic divergence typically associated with sister species, con- Materials and Methods geners, and confamilial genera (the comparisons ana- Sequences Employed lyzed here) usually are in a range in which the cytb gene Cytb sequences were retrieved from GenBank re- is phylogenetically informative and unlikely to be se- lease 103.0, which includes all sequences entered prior verely compromised by saturation effects involving su- to October 9, 1997. A total of 2,821 cytb sequences of perimposed nucleotide substitutions (Moritz, Dowlilng, length $ 200 bp were found for species classi®ed in the and Brown 1987; Meyer 1994). Finally, it is of interest subphylum Vertebrata. When multiple haplotypes for a to compare distance trends from homologous DNA se- species were recorded, only the longest of the coding sequences was analyzed (in the event of a tie, one se- 1 Present address: Hopkins Marine Station, Stanford University. quence was chosen at random to represent that species). Key words: cytochrome b, mitochondrial DNA, genetic diver- Two unpublished sequences were found to have multiple gence, vertebrates, comparative molecular evolution. insertions and deletions when compared with congeneric Address for correspondence and reprints: John C. Avise, Depart- sequences. They also had multiple stop codons in all ment of Genetics,University of Georgia, Athens, Georgia 30602. E- three reading frames and thus were excluded from fur- mail: [email protected]. ther analysis as probable pseudogenes. The culled data Mol. Biol. Evol. 15(11):1481±1490. 1998 set represented 1,832 cytb sequences (1 per species). A q 1998 by the Society for Molecular Biology and Evolution. ISSN: 0737-4038 list of the species and GenBank accession numbers for 1481 1482 Johns and Avise these sequences is available from the authors upon re- logenetic guesses on scores of groups [and in any event, quest. in many cases, no obvious outgroup sequences were Sequence comparisons involving congeners were available].) Of course, these analyses may falsely ear- made for any genus represented by two or more species mark some taxa as sister species merely because inter- in the data bank. Similarly, analyses of confamilial gen- mediate sequences or species were missing from the da- era involved the use of a single sequence per genus for tabase. Nonetheless, the approach is useful for compar- any taxonomic family represented in the data by two or ative purposes when viewed conservatively as providing more genera. maximum estimates of sister species genetic distances. These genetic distances (which are independent of Genetic Distance Calculations one another in value) were accumulated across provi- Cytb gene sequences were aligned using pileup in sional sister species pairs for each vertebrate group. The the GCG package (Genetics Computer Group Inc.). Ge- resulting means in the frequency distributions were netic distances (p) were estimated for all pairwise com- compared statistically using Kruskal-Wallis tests. parisons using Kimura's (1980) two-parameter model as implemented in PAUP* (Swofford 1998). Altogether, Results 7,699 pairwise sequence comparisons were conducted. Congeneric Species and Confamilial Genera Statistical Analyses Figures 1±4 plot on a common scale the compila- Separate analyses were performed on sister species, tions of cytb genetic distances for congeneric species (in species within a genus, and genera within a taxonomic 288 genera) within each of the ®ve major vertebrate family. Various statistical procedures were employed to classes. Bird species typically show relatively small val- determine if the means in the distributions of sequence ues, whereas the genetic distance distributions of con- divergence estimates at a given taxonomic rank differed generic ®shes, reptiles, and amphibians show larger var- signi®cantly across major vertebrate groups. To avoid iances and include some estimates that far surpass any the complications of nonindependence associated with of those recorded for birds (®g. 5). Assayed mammalian multiple pairwise estimates from a single phylogeny, congeners generally appear intermediate in these re- only the mean p value for a genus (in analyses of con- gards. generic species) or for a family (in analyses of confam- At the level of congeneric species, the frequency ilial genera) was included in the statistical tests. Rela- distributions of mean sequence divergence estimates tively few cytb sequences have been reported for am- (®g. 5) are highly signi®cantly different among the ma- phibians and reptiles, so in some of the statistical anal- jor vertebrate classes examined (P , 0.0001; table 1). yses (where mentioned), these organisms were A multiple-comparisons test indicates that this outcome arti®cially pooled as herpetofauna. results primarily from signi®cant differences (P , 0.05) The distributions of mean sequence divergence es- between the birds and the other major vertebrate groups, timates within groups sometimes were signi®cantly non- and that these other groups show no signi®cant differ- normal, so nonparametric rank sums tests (Kruskal and ences from one another at this taxonomic level (table Wallis 1952) using the x2 approximation were per- 1). formed to assess differences in the means of the histo- Comparable summaries for confamilial genera are grams of mean p among the vertebrate groups. Where a presented in ®gure 5. These genetic distance distribu- signi®cant result warranted further inspection, Kruskal- tions were also signi®cantly different among the major Wallis multiple-comparisons tests were used to deter- vertebrate classes (P , 0.0001; table 1). This outcome mine which means
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