Trees within trees: genes and species, molecules and morphology.

The construction and interpretation of gene trees is fundamental in molecular system- atics. If the gene is defined in a historical (coalescent) sense, there can be multiple gene trees within the single contiguous set of nucleotides, and attempts to construct a single tree for such a sequence must deal with homoplasy created by conflict among divergent histories. On a larger scale, incongruence is expected among gene tree topologies at different loci of individuals within sexually reproducing species, and it has been suggested that this discordance can be used to delimit species. A practical concern for such topological methods is that polymorphisms may be maintained through numerous cladogenic events; this polymorphism problem is less of a concern for nontopological approaches to species delimitation using molecular data. Although a central theoretical concern in molecular systematics is discordance between a given gene tree and the true "species tree," the primary empirical problem faced in reconstructing taxic phylogeny is incongruence among the trees inferred from different sequences. Linkage relationships limit char- acter independence and thus have important implications for handling multiple data sets in phy- logenetic analysis, particularly at the species level, where incongruence among different histori- cally associated loci is expected. Gene trees can also be reconstructed for loci that influence phenotypic characters, but there is at best a tenuous relationship between phenotypic homoplasy and homoplasy in such gene trees. Nevertheless, expression patterns and orthology relationships of genes involved in the expression of phenotypes can in theory provide criteria for homology assessment of morphological characters. (Gene trees; homoplasy; linkage; morphology; orthology; phylogeny; species delimitation.) Page (1993, 1994) summarized several ways in which trees from one hierarchical level may "include" historically associated trees from a lower level. The trees of the lowest hierarchical and organizational lev- el, the gene, are discussed here. Gene trees are fundamental to molecular systematics, i.e., to systematics generally. The primary use of such trees, constructed from DNA sequence variation at individual genetic loci, is to infer phylogenies of the taxa bearing those genes. As such, genes are lit- tle more than collections of individual nu- cleotides, each assumed to be an indepen- dent and representative character for organismal phylogeny reconstruction. The fact that systematists are speaking of "gene trees" at all and distinguishing them from trees of taxic relationships rep- resents a significant advance over earlier— not long past—ways of thinking about mo- lecular systematics. The full implications of that distinction, necessitated at each taxo- nomic level by different but often overlap- ping biological processes, are still being elucidated and remain to be incorporated into the day-to-day work of systematics. Two aspects of "inclusion" that involve gene trees are explored here. The first is gene flow, which in sexually reproducing organisms brings together lineages with different histories. Gene trees become his- torically associated as genes are united in different combinations within the genomes of individual organisms. Two hierarchical levels are involved: the lower level is that of the gene, and the higher level is that of the organism. The presence of different al- leles at a locus provides the substrate for effective recombination. Within a contigu- ous set of nucleotides composing a struc- tural gene, recombination may produce new alleles that are phylogenetic mosaics, with significant implications for gene tree construction. Above the organizational lev- el of single loci, recombinational mecha- nisms (crossing over, gene conversion, in- dependent assortment) permit individual loci to evolve independently and poten- tially to track different histories. An im-