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Intraspecific Phylogenetics JOURNAL OF VIROLOGY, Apr. 1995, p. 2351–2356 Vol. 69, No. 4 0022-538X/95/$04.0010 Copyright q 1995, American Society for Microbiology Intraspecific Phylogenetics: Support for Dental Transmission of Human Immunodeficiency Virus KEITH A. CRANDALL* Department of Zoology, University of Texas at Austin, Austin, Texas 78712-1064 Received 25 August 1994/Accepted 10 January 1995 A new method to estimate within-species gene genealogies was used to establish linkages among individuals associated with the Florida dental human immunodeficiency virus transmission case. Phylogenetic relation- ships were estimated from 103 nucleotide sequences from the V3 region of the env gene representing the Florida dentist, eight of his seropositive patients, and many local controls. The cladogram estimation procedure supports linkages among individuals within the previously described dental clade, whereas local controls and other patients form independent networks or are outliers in the main network, indicating more distant evolutionary relationships. A nested statistical analysis also indicates significant cohesion of the dental clade group. In a recent correspondence, DeBry et al. (5) commented on est statistical power when the number of differences between the need for an appropriate framework within which one can any pair of sequences is few, as is typically the case with test the hypothesis of human immunodeficiency virus (HIV) intraspecific data sets. Traditional methods (e.g., parsimony) transmission. DeBry et al. (5) criticized the original analysis of were developed to estimate phylogenetic relationships over an HIV transmission case in Florida for using an inappropriate greater time spans, in which the number of variable sites is model of evolution (and phylogeny reconstruction technique) large relative to the number of shared sites. Huelsenbeck and and inadequate sampling of local controls. They reexamined Hillis (11) have shown that these traditional methods (includ- the conclusion reached by Ou et al. (12) that a Florida dentist ing weighted and unweighted parsimony, UPGMA, and neigh- infected five of his eight HIV type 1 (HIV-1)-seropositive bor joining) all perform poorly when few (,100 bp) differences patients using an alternative model of evolution and additional exist among sequences. Crandall (1), however, has shown that controls. The phylogenetic analysis by DeBry et al. (5) indi- the method of Templeton et al. (21) performs well and out- cated no resolution between the null hypothesis of indepen- performs bootstrapping with maximum parsimony, even at dent acquisition of HIV-1 versus the alternative of infection via higher levels of divergence, when few characters are available the Florida dentist. for analysis. Crandall et al. (4) have detailed the advantages to Both the analyses by Ou et al. (12) and DeBry et al. (5) were the intraspecific cladogram estimation procedure relative to based on variations of the maximum parsimony procedure for traditional methods, including the ability to account for recom- phylogeny reconstruction (18). This procedure establishes re- bination within a data set, accommodation of multifurcating lationships based on shared derived characters and was devel- relationships, and the acceptance of extant ancestral se- oped for estimating higher-level systematic relationships. Un- quences. In addition, this procedure provides a statistical fortunately, many of the assumptions of the parsimony framework for testing hypotheses of associations for both con- procedure do not hold for population genetic data. For exam- tinuous and categorical data (20, 22). ple, population genetic data are not necessarily strictly bifur- The purpose of this paper is to present this alternative pro- cating. They can include reticulations which result in lack of cedure for estimating intraspecific gene genealogies and dem- resolution when using a maximum parsimony procedure. Pop- onstrate its utility in reconstructing relationships of closely ulation genetic data, including HIV-1 sequences, can be sub- related sequences and its facility for hypothesis testing based ject to recombination (14). Traditional phylogeny reconstruc- on the cladogram structure. I have reanalyzed the HIV se- tion techniques do not take into consideration the possibility of quences of Ou et al. (12) with the addition of new sequences recombination and therefore will give erroneous results if re- from DeBry et al. (5) using this procedure. The resulting cla- combination has occurred within the aligned sequences. Fi- dogram indicates statistical support for the dental clade as nally, individual sequences are typically differentiated by few originally concluded by Ou et al. (12). Furthermore, a nested nucleotide substitutions. Because maximum parsimony re- statistical analysis gives further support for the dental clade. quires characters to be shared among variant sequences in order to be informative, the data set available for phylogeny reconstruction is very limited with closely related individuals, MATERIALS AND METHODS resulting in a lack of resolution of phylogenetic relationships. A method that takes into account these special consider- HIV sequences. A total of 103 HIV nucleotide sequences from the V3 region ations for within-species cladogram estimation has recently of the env gene were obtained from GenBank for phylogenetic analysis. These sequences include 86 variant sequences listed by Ou et al. (12) and 17 additional been developed. The intraspecific cladogram estimation pro- local controls offered by DeBry et al. (5). The sequences were aligned with cedure of Templeton et al. (21) was designed to have its great- CLUSTAL V. Because of the high levels of variability within the V3 region, positional homology was suspect in a number of aligned positions. These posi- tions were eliminated from analysis, resulting in total of 240 nucleotide positions from the V3 region. The alignment used in this analysis is available from the * Mailing address: Department of Zoology, University of Texas, author upon request. This represents the largest data set used to analyze the Austin, TX 78712-1064. Phone: (512) 471-5661. Fax: (512) 471-9651. Florida dental transmission hypothesis to date. Because of the resolving power of Electronic mail address: [email protected]. the method of Templeton et al. (21), multiple sequences per individual can be 2351 2352 CRANDALL J. VIROL. FIG. 1. A hypothetical example demonstrating the parsimony concept used by the cladogram estimation procedure. Given a nucleotide difference between sequences, noted in the box, the probability that a multiple mutation (the non- parsimonious state) has occurred is greater for sequence pairs that share fewer sites, pair C and D, than for those that share more sites, pair A and B. used without a loss of resolution. Thus, all complete sequences available for each patient and the dentist were used in this study. FIG. 2. A demonstration of the nesting procedure with missing intermedi- Cladogram estimation. The cladogram estimation procedure of Templeton et ates. The nesting begins with the tip variants, those with only a single mutation al. (21) estimates the set of cladograms that portray connections among variant connection, and proceeds by nesting n-step clades separated by n 1 1 mutational sequences where these connections have a high cumulative probability ($0.95) of steps in the interior direction. Each variant sequence forms a zero-step clade. Six being true, thereby constructing a plausible set of alternative cladograms. This one-step clades are formed by joining the zero-step clades separated by one estimation algorithm is based on a parsimony criterion with a statistical proce- mutational difference (each arrow represents a single mutational step). The dure to evaluate the limits of the parsimony assumption. Under consideration by procedure is repeated recursively until one reaches the level at which the next the method is the number of mutational events causing a single nucleotide round of nesting would unite the entire cladogram into a single category. difference between two variant sequences, with a difference caused by a single mutational event being the parsimonious state and a difference cause by multiple mutational events being the nonparsimonious state (Fig. 1). Thus, the term parsimony refers to the minimum number of mutations separating two individual differing by j sites and sharing m sites have a parsimonious relationship (i.e., no sequences rather than a global minimum tree length based on shared derived unobserved mutations at any site) is then estimated by characters. The statistical evaluation of the limits of parsimony asks the following ques- j ˆ tion: given that two variant sequences differ at j nucleotide positions and share m Pj 5 P~1 2 qi! (3) positions, what is the probability that multiple mutational events have occurred i51 within one or more of the j sites differentiating the two sequences? If the probability of multiple mutations is high (i.e., P . 0.95), then the parsimony To implement this method, pairwise distances from the set of aligned HIV criterion is invalid. Templeton et al. (21) have developed a population genetic sequences were calculated with PAUP’s ‘‘show distance matrix’’ option (17). model to evaluate this probability. They first condition their model on an index Equation 3 was then used to calculate the probability of parsimonious connec- site, the oldest polymorphic site. Then, the total probability that two sequences tions between variant sequences
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