Predicting nuclear gene coalescence from mitochondrial data: the three-times rule.

Coalescence theory predicts when genetic drift at nuclear loci will result in fixation of sequence differences to produce monophyletic gene trees. However, the theory is difficult to apply to particular taxa because it hinges on genetically effective population size, which is generally unknown. Neutral theory also predicts that evolution of monophyly will be four times slower in nuclear than in mitochondrial genes primarily because genetic drift is slower at nuclear loci. Variation in mitochondrial DNA (mtDNA) within and between species has been studied extensively, but can these mtDNA data be used to predict coalescence in nuclear loci? Comparison of neutral theories of coalescence of mitochondrial and nuclear loci suggests a simple rule of thumb. The "three-times rule" states that, on average, most nuclear loci will be monophyletic when the branch length leading to the mtDNA sequences of a species is three times longer than the average mtDNA sequence diversity observed within that species. A test using mitochondrial and nuclear intron data from seven species of whales and dolphins suggests general agreement with predictions of the three-times rule. We define the coalescence ratio as the mitochondrial branch length for a species divided by intraspecific mtDNA diversity. We show that species with high coalescence ratios show nuclear monophyly, whereas species with low ratios have polyphyletic nuclear gene trees. As expected, species with intermediate coalescence ratios show a variety of patterns. Especially at very high or low coalescence ratios, the three-times rule predicts nuclear gene patterns that can help detect the action of selection. The three-times rule may be useful as an empirical benchmark for evaluating evolutionary processes occurring at multiple loci.

Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin.

Bindin is a gamete recognition protein of sea urchins that mediates species-specific attachment of sperm to an egg-surface receptor during fertilization. Sequences of bindin from closely related urchins show fixed species-specific differences. Within species, highly polymorphic bindin alleles result from point substitution, insertion/deletion, and recombination. Since speciation, positive selection favoring allelic variants has generated diversity in bindin polypeptides. Intraspecific bindin variation can be tolerated by the egg receptor, which suggests functional parallels between this system and other flexible recognition systems, including immune recognition. These results show that polymorphism in mate recognition loci required for rapid evolution of sexual isolation can arise within natural populations.

Multiple origins of a spider radiation in Hawaii.

The Hawaiian Islands are renowned for some of the most spectacular species radiations in the world. Most of these radiations have been attributed to single colonization events, although the evidence supporting monophyletic origins is often poorly resolved and/or ambiguous. Without a concrete understanding of the origins of species radiations, it is impossible to understand the phylogenetic pattern of species proliferation or the spectrum of morphological, ecological, and behavioral modifications attributable to a single colonist. In this study we examined the species radiation of the spider genus Tetragnatha in Hawaii. Unlike their mainland congeners, the Hawaiian Tetragnatha are extremely diverse in morphology, ecology, and behavior. We tested whether this diversity arose from a single or multiple colonization events. We coupled morphological (37 characters) and molecular (sequence from the 12S ribosomal subunit of mitochondrial DNA) approaches to assess the phylogenetic position of the Hawaiian Tetragnatha relative to continental congeners and to examine evidence for monophyly. We provide evidence that the Hawaiian Tetragnatha emanate from multiple origins. At least two independent species radiations, the "spiny-leg" clade and the web-building species Tetragnatha stelarobusta and Tetragnatha acuta, have arisen from one or more founder events. Two additional natural colonizations have resulted in the establishment of non-speciose lineages, as represented by Tetragnatha hawaiensis and Doryonychus raptor.