Molecular Ecology (2001) 10 , 779–791© 2001 Blackwell Science Ltd Blackwell Science, Ltd Using phylogeographic analyses of gene trees to test species status and processes ALAN R. TEMPLETON Department of Biology, Campus Box 1137, Washington University, St. Louis, Missouri 63130–4899, USA AbstractA gene tree is an evolutionary reconstruction of the genealogical history of the genetic vari-ation found in a sample of homologous genes or DNA regions that have experienced littleor no recombination. Gene trees have the potential of straddling the interface betweenintra- and interspecific evolution. It is precisely at this interface that the process of speciationoccurs, and gene trees can therefore be used as a powerful tool to probe this interface. Oneapplication is to infer species status. The cohesion species is defined as an evolutionarylineage 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 rigorouslyand objectively by using gene trees. First, an overlay of geography upon the gene tree isused to test the null hypothesis that the sample is from a single evolutionary lineage. Thisphase of testing can indicate that the sampled organisms are indeed from a single lineageand therefore a single cohesion species. In other cases, this null hypothesis is not rejected dueto a lack of power or inadequate sampling. Alternatively, this null hypothesis can be rejectedbecause two or more lineages are in the sample. The test can identify lineages even whenhybridization and lineage sorting occur. Only when this null hypothesis is rejected is therethe potential for more than one cohesion species. Although all cohesion species are evolu-tionary lineages, not all evolutionary lineages are cohesion species. Therefore, if the firstnull hypothesis is rejected, a second null hypothesis is tested that all lineages are genetic-ally exchangeable and/or ecologically interchangeable. This second test is accomplishedby direct contrasts of previously identified lineages or by overlaying reproductive and/orecological data upon the gene tree and testing for significant transitions that are concordantwith the previously identified lineages. Only when this second null hypothesis is rejectedis 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 thatautomatically yields much insight into the process of speciation. When one or more of thenull hypotheses cannot be rejected, this procedure also provides specific guidance forfuture 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 wouldlike their concepts to be as general, applicable and theoret-ically significant as possible. With respect to species concepts,these goals are often in conflict with each other, leadingHull (1997, 1999) to conclude that there is no ideal speciesconcept and that a plurality of species concepts may beneeded. One of the species concepts evaluated by Hull isthe cohesion species concept (Templeton 1989). A cohesionspecies is an evolutionary lineage whose boundaries arisefrom the genetic and ecological forces that create cohesivereproductive communities (Templeton 1998a, 1999).An evolutionary lineage is a reproducing populationwith sufficient historical continuity (ancestral-descendant Correspondence: Alan R. Templeton. Fax: 1 314 935 4432; E-mail:[email protected] MEC1199.fm Page 779 Monday, March 12, 2001 6:55 PM780 A. R. TEMPLETON © 2001 Blackwell Science Ltd, Molecular Ecology , 10, 779–791 relationships) to have its own evolutionary trajectories andtendencies (an operational definition will be given later).The cohesion concept scored well by Hull’s first criteriaof generality. All life evolves and forms lineages, so defin-ing a species as an evolutionary lineage connects the cohe-sion concept to a true biological universal. In particular,Hull points out that the major impediments to universalityof most species concepts are the opposite challengesof asexual reproduction and hybridization. Both sexualand asexual taxa can define evolutionary lineages, so thecohesion concept applies to all life on this planet and notjust the small subset that reproduces in a manner similar tohumans. Moreover, a novel evolutionary lineage can startfrom a stabilized or recombinant hybridization eventbetween species (Templeton 1981), a fact overwhelminglydocumented 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 & Hebert1994; Schartl et al . 1995; Carmona et al . 1997; Kenyon 1997;Grant & Grant 1998; Parris 1999; Vila & Wayne 1999). Thecohesion species concept can embrace these lineagesfounded by hybridization events (Templeton 1989). More-over, cohesion lineages can show limited hybridizationwithout losing their lineage status by using explicit, object-ive and quantifiable criteria (Templeton 1994a). Hence, thecohesion species concept acknowledges hybridization asan important and potentially creative force in speciation.The cohesion concept did not score well with the cri-terion of applicability under Hull’s reckoning. This is notsurprising, as Hull (1997, 1999) only cites Templeton (1989)when discussing the cohesion concept. That paper wasdesigned to introduce the cohesion concept into the evolu-tionary literature, but did not nor was intended to addressthe issue of making the concept operational. The issueof applicability was addressed in subsequent papers(Templeton 1994a, 1998a, 1999), none of which were con-sidered by Hull (1997, 1999). These subsequent papersshow with worked examples that the cohesion conceptcan be rephrased as a set of testable null hypotheses. Theoperational implementation of the cohesion conceptrequires data gathering techniques (e.g. DNA sequencing,restriction site mapping, etc.) that are now readily avail-able. Given that virtually all data sets represent a sampleand that measurement errors are possible, null hypothesesare formulated that must be rejected with statistical sig-nificance before inferring a cohesion
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