Predicting Nuclear Gene Coalescence From Mitochondrial Data: The Three-Times Rule

Abstract

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.

The role of subspecies in obscuring avian biological diversity and misleading conservation policy

“…Although the use of a single molecular marker such as mtDNA might result in mistaken intraspecific histories (Avise & Wollenberg 1997), mtDNA gene trees routinely recover significant divisions in avian species; rarely have nuclear markers shown that such divisions are incorrect (Avise 2000). Furthermore, because of longer coalescence times, nuclear markers such as microsatellites are unlikely to capture genetic diversity not also evident in mtDNA gene trees (Palumbi et al 2001). However, it will be important to confirm the findings reported here with nuclear loci.…”

Different patterns of colonization of Oxalis alpina in the Sky Islands of the Sonoran desert via pollen and seed flow

“…The ANCOVA analysis of microsatellite data showed a marginally significant effect of latitude on the H E parameter, suggesting that northern migrations have left a weaker signature on the patterns of diversity on the nuclear genome, in contrast to the chloroplast genome. This pattern is probably the consequence of the lower effective population size of cytoplasmic genes in comparison with nuclear genes (Birky, Fuerst, & Maruyama, 1989; Palumbi, Cipriano, & Hare, 2001). …”

“…Therefore, gene flow should be higher for nuclear markers carried by pollen than for organellar markers carried by seeds and may explain the detection of more genetically differentiated groups of populations using cpDNA than nuclear markers. Divergent patterns of genetic structure might also be explained by the more rapid coalescence of uniparentally inherited haploid alleles in mitochondrial or chloroplast DNA that have smaller effective population sizes than most nuclear loci (Birky et al., 1989; Palumbi et al., 2001). Smaller effective population size for organellar DNA accelerates the processes of genetic drift in neutral markers, producing more rapid genetic divergence among populations (Palumbi et al., 2001).…”

“…Divergent patterns of genetic structure might also be explained by the more rapid coalescence of uniparentally inherited haploid alleles in mitochondrial or chloroplast DNA that have smaller effective population sizes than most nuclear loci (Birky et al., 1989; Palumbi et al., 2001). Smaller effective population size for organellar DNA accelerates the processes of genetic drift in neutral markers, producing more rapid genetic divergence among populations (Palumbi et al., 2001). These processes may in part explain the strong subdivision observed through cpDNA in O. alpina , where five genetic groups of populations were detected.…”

Impact of Ice Ages on the genetic structure of trees and shrubs

“…So at migration/drift equilibrium the difference between the two is expected to be relatively minor. Nevertheless, Palumbi et al (2001) showed that, under complete separation, organelles will reach this equilibrium much faster than nuclear markers, whereas stochasticity further blurs the difference (Hudson & Turelli 2003). More complex histories could of course be simulated, but simplicity of the model is an important criterion when selecting among competing hypotheses (Knowles & Maddison 2002).…”