Phylogenetics of Darwin's finches: Paraphyly in the tree-finches, and two divergent lineages in the Warbler finch

ABSTRACT.-The Galapagos Darwin's finches (Geospizinae) have been classified as three major groups based on morphology and behavior: ground-finches, tree-finches, and the Warbler Finch (Certhidea olivacea). Little is known about the evolutionary relationships within and among these groups, which is partly due to the lack of a phylogeny based on molecular sequence data. We used mitochondrial sequence data to reconstruct a phylogeny of Darwin's finches. These data show that within the tree-finches, only one genus is conclusively monophyletic, and another is conclusively paraphyletic. It may be appropriate to uphold the classification of the tree-finches into two genera. The Warbler Finch complex is paraphyletic, as revealed by two divergent genetic lineages contained within this species. Stochastic lineage sorting within relatively recently diverged species and interspecific and intergeneric hybridization are the two most likely explanations for the sharing of haplotypes among taxa. Received 3 March 1998, accepted 6 November 1998.

ADAPTIVE RADIATION refers to the process in which one species evolves into numerous species over a relatively short period of time. The question of how this occurs is fundamental to studies of evolution and speciation and has been at the heart of considerable research (e.g. DeSalle et al. 1987, Sang et al. 1994, Losos 1995, Tarr and Fleischer 1995, Cameron et al. 1996, Radtkey 1996, Shaw 1996). Perhaps the most famous ongoing study of adaptive radiation involves Darwin's finches (Geospizinae). More than 100 years of research have been conducted on Darwin's finches, yet, many questions about their evolutionary history remain unanswered. A glaring omission in this field of study is the lack of a sequence-based phylogeny. A molecular data set for the group will yield further insight into a number of aspects of evolution and speciation, including adaptive radiation.

The subfamily Geospizinae comprises 14 nominate species, 13 of which inhabit the Galapagos Archipelago. Darwin's finches have been divided into three groups based on morphology and behavior: ground-finches, treefinches, and the Warbler Finch (Certhidea olivacea; Table 1). The ground-finches (Geospiza) comprise one genus and six species that are finch-like in appearance, particularly with respect to their bills, and spend much of their time foraging on the ground. The tree-finches (Camarhynchus, Platyspiza, and Cactospiza) comprise six species, but the number of genera oscillates between one and three (see below). These six species have bills intermediate to those of ground-finches and the Warbler Finch, and although they occasionally forage on the ground in a manner similar to ground-finches, they spend much of their time in foliage and vegetation exhibiting behavior similar to that of the Warbler Finch. The Warbler Finch is a monotypic genus consisting of eight subspecies. True to its name, this species closely resembles a warbler with respect to its small size, slender bill, and habit of gleaning animal food from foliage.

Morphological, behavioral, and allozyme data (Lack 1947, Yang and Patton 1981, Schluter 1984) all agree with the division of the Galapagos finches into the three groups outlined above. However, little is known about the phylogenetic associations among the groups, and even less is known about the relationships of genera, species, and subspecies within each group. The only published genetic studies of Darwin's finches are based on allozyme data (Ford et al. 1974, Yang and Patton 1981, Polans 1983) that lack the level of resolution necessary to infer many phylogenetic relationships. In this paper, we use mitochondrial sequence data to clarify unanswered questions pertaining to the phylogeny of Darwin's finches.

First, we address evolutionary relationships of the three groups. Existing phylogenies consistently treat the Warbler Finch as the basal taxon, but the positions of the tree-finches and ground-finches remain equivocal. The latter groups generally are treated as monophyletic sister groups (Lack 1947, Schluter 1984); however, it has also been suggested that the treefinches are ancestral to the ground-finches (Stern and Grant 1996), and under this scenario it is possible that the tree-finches are a paraphyletic group. Prior to investigating evolutionary relationships within the tree-finches, we wished to ascertain whether taxonomic separation of the tree-finches and ground-finches, based on morphological data, was reflected by their DNA sequences. Because Darwin's finches underwent adaptive radiation relatively recently (Yang and Patton 1981), there may have been insufficient time for complete lineage sorting to have occurred following speciation, which could result in the sharing of haplotypes among species (Neigel and Avise 1986). In addition, hybridization has been documented in Darwin's finches (Grant 1986), and this may lead to introgression of mitochondrial haplotypes from one species to another (Tegelstrom 1987). We reconstructed a phylogeny of the three groups using mitochondrial sequence data, which allowed us to infer relative levels of genetic relatedness within and among the tree-finches, ground-finches, and the Warbler Finch.