MEC1199 fm Page 779 Monday March 12 2001 6 55 PM Molecular Ecology 2001 10 779 791 Using phylogeographic analyses of gene trees to test species status and processes Blackwell Science Ltd ALAN R TEMPLETON Department of Biology Campus Box 1137 Washington University St Louis Missouri 63130 4899 USA Abstract A gene tree is an evolutionary reconstruction of the genealogical history of the genetic variation found in a sample of homologous genes or DNA regions that have experienced little or no recombination Gene trees have the potential of straddling the interface between intra and interspecific evolution It is precisely at this interface that the process of speciation occurs and gene trees can therefore be used as a powerful tool to probe this interface One application is to infer species status The cohesion species is defined as an evolutionary lineage or set of lineages with genetic exchangeability and or ecological interchangeability This species concept can be phrased in terms of null hypotheses that can be tested rigorously and objectively by using gene trees First an overlay of geography upon the gene tree is used to test the null hypothesis that the sample is from a single evolutionary lineage This phase of testing can indicate that the sampled organisms are indeed from a single lineage and therefore a single cohesion species In other cases this null hypothesis is not rejected due to a lack of power or inadequate sampling Alternatively this null hypothesis can be rejected because two or more lineages are in the sample The test can identify lineages even when hybridization and lineage sorting occur Only when this null hypothesis is rejected is there the potential for more than one cohesion species Although all cohesion species are evolutionary lineages not all evolutionary lineages are cohesion species Therefore if the first null hypothesis is rejected a second null hypothesis is tested that all lineages are genetically exchangeable and or ecologically interchangeable This second test is accomplished by direct contrasts of previously identified lineages or by overlaying reproductive and or ecological data upon the gene tree and testing for significant transitions that are concordant with the previously identified lineages Only when this second null hypothesis is rejected is a lineage elevated to the status of cohesion species By using gene trees in this manner species can be identified with objective a priori criteria with an inference procedure that automatically yields much insight into the process of speciation When one or more of the null hypotheses cannot be rejected this procedure also provides specific guidance for future work that will be needed to judge species status Keywords fragmentation haplotype tree hybridization nested clade analysis phylogeography species Received 4 June 2000 revision received 7 September 2000 accepted 7 September 2000 Introduction Hull 1997 1999 pointed out that scientists ideally would like their concepts to be as general applicable and theoretically significant as possible With respect to species concepts these goals are often in conflict with each other leading Correspondence Alan R Templeton Fax 1 314 935 4432 E mail temple a biology wustl edu 2001 Blackwell Science Ltd Hull 1997 1999 to conclude that there is no ideal species concept and that a plurality of species concepts may be needed One of the species concepts evaluated by Hull is the cohesion species concept Templeton 1989 A cohesion species is an evolutionary lineage whose boundaries arise from the genetic and ecological forces that create cohesive reproductive communities Templeton 1998a 1999 An evolutionary lineage is a reproducing population with sufficient historical continuity ancestral descendant MEC1199 fm Page 780 Monday March 12 2001 6 55 PM 780 A R T E M P L E T O N relationships to have its own evolutionary trajectories and tendencies an operational definition will be given later The cohesion concept scored well by Hull s first criteria of generality All life evolves and forms lineages so defining a species as an evolutionary lineage connects the cohesion concept to a true biological universal In particular Hull points out that the major impediments to universality of most species concepts are the opposite challenges of asexual reproduction and hybridization Both sexual and asexual taxa can define evolutionary lineages so the cohesion concept applies to all life on this planet and not just the small subset that reproduces in a manner similar to humans Moreover a novel evolutionary lineage can start from a stabilized or recombinant hybridization event between species Templeton 1981 a fact overwhelmingly documented in the botanical literature Rieseberg 1997 and found in the animal literature as well e g Vyas et al 1990 DeMarais et al 1992 Bullini 1994 Dufresne Hebert 1994 Schartl et al 1995 Carmona et al 1997 Kenyon 1997 Grant Grant 1998 Parris 1999 Vila Wayne 1999 The cohesion species concept can embrace these lineages founded by hybridization events Templeton 1989 Moreover cohesion lineages can show limited hybridization without losing their lineage status by using explicit objective and quantifiable criteria Templeton 1994a Hence the cohesion species concept acknowledges hybridization as an important and potentially creative force in speciation The cohesion concept did not score well with the criterion of applicability under Hull s reckoning This is not surprising as Hull 1997 1999 only cites Templeton 1989 when discussing the cohesion concept That paper was designed to introduce the cohesion concept into the evolutionary literature but did not nor was intended to address the issue of making the concept operational The issue of applicability was addressed in subsequent papers Templeton 1994a 1998a 1999 none of which were considered by Hull 1997 1999 These subsequent papers show with worked examples that the cohesion concept can be rephrased as a set of testable null hypotheses The operational implementation of the cohesion concept requires data gathering techniques e g DNA sequencing restriction site mapping etc that are now readily available Given that virtually all data sets represent a sample and that measurement errors are possible null hypotheses are formulated that must be rejected with statistical significance before inferring a cohesion species Such use of statistical tests is a widespread operational procedure in virtually all science Finally the criteria for
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