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Estimating divergence dates and substitution rates in the Drosophila phylogeny.

Obbard DJ, Maclennan J, Kim KW, Rambaut A, O'Grady PM, Jiggins FM - Mol. Biol. Evol. (2012)

Bottom Line: Surprisingly, our estimate for the date for the most recent common ancestor of the genus Drosophila based on mutation rate (25-40 Ma) is closer to being compatible with independent fossil-derived dates (20-50 Ma) than are most of the Hawaiian-calibration models and also has smaller uncertainty.Potential problems with the Hawaiian calibration may arise from systematic variation in the molecular clock due to the long generation time of Hawaiian Drosophila compared with other Drosophila and/or uncertainty in linking island formation dates with colonization dates.As either source of error will bias estimates of divergence time, we suggest mutation rate estimates be used until better models are available.

View Article: PubMed Central - PubMed

Affiliation: Institute of Evolutionary Biology, and Centre for Infection Immunity and Evolution, University of Edinburgh, Edinburgh, United Kingdom. darren.obbard@ed.ac.uk

ABSTRACT
An absolute timescale for evolution is essential if we are to associate evolutionary phenomena, such as adaptation or speciation, with potential causes, such as geological activity or climatic change. Timescales in most phylogenetic studies use geologically dated fossils or phylogeographic events as calibration points, but more recently, it has also become possible to use experimentally derived estimates of the mutation rate as a proxy for substitution rates. The large radiation of drosophilid taxa endemic to the Hawaiian islands has provided multiple calibration points for the Drosophila phylogeny, thanks to the "conveyor belt" process by which this archipelago forms and is colonized by species. However, published date estimates for key nodes in the Drosophila phylogeny vary widely, and many are based on simplistic models of colonization and coalescence or on estimates of island age that are not current. In this study, we use new sequence data from seven species of Hawaiian Drosophila to examine a range of explicit coalescent models and estimate substitution rates. We use these rates, along with a published experimentally determined mutation rate, to date key events in drosophilid evolution. Surprisingly, our estimate for the date for the most recent common ancestor of the genus Drosophila based on mutation rate (25-40 Ma) is closer to being compatible with independent fossil-derived dates (20-50 Ma) than are most of the Hawaiian-calibration models and also has smaller uncertainty. We find that Hawaiian-calibrated dates are extremely sensitive to model choice and give rise to point estimates that range between 26 and 192 Ma, depending on the details of the model. Potential problems with the Hawaiian calibration may arise from systematic variation in the molecular clock due to the long generation time of Hawaiian Drosophila compared with other Drosophila and/or uncertainty in linking island formation dates with colonization dates. As either source of error will bias estimates of divergence time, we suggest mutation rate estimates be used until better models are available.

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Models linking speciation with coalescence. Panels (a–c) depict the coalescence of lineages (black lines) sampled at time t0 from three island-endemic species (labeled 1, 2, and 3). In this idealized model, speciation events can be associated with the colonization of island 2 from island 3 at time t2 and the colonization of island 1 from island 2 at time t1. Associating coalescence with speciation is less easy. In panel (a), population sizes are extremely small (depicted by the width of the gray background), so that coalescence happens extremely rapidly and the coalescence date of sequences sampled from islands 1 and 2 can be approximated to the date at which island 1 was colonized. In panel (c) within-island population sizes are effectively infinite, but the bottleneck at colonization is very tight. Thus, coalescence does not occur on the island until the colonization bottleneck is reached, when coalescence becomes very rapid. Under this model, the coalescence date of island lineages 1 and 2 can be approximated by the formation of island 2 at time t2. In panel (b), population sizes are intermediate, and coalescence time is determined by the effective population size on the ancestral island.
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mss150-F1: Models linking speciation with coalescence. Panels (a–c) depict the coalescence of lineages (black lines) sampled at time t0 from three island-endemic species (labeled 1, 2, and 3). In this idealized model, speciation events can be associated with the colonization of island 2 from island 3 at time t2 and the colonization of island 1 from island 2 at time t1. Associating coalescence with speciation is less easy. In panel (a), population sizes are extremely small (depicted by the width of the gray background), so that coalescence happens extremely rapidly and the coalescence date of sequences sampled from islands 1 and 2 can be approximated to the date at which island 1 was colonized. In panel (c) within-island population sizes are effectively infinite, but the bottleneck at colonization is very tight. Thus, coalescence does not occur on the island until the colonization bottleneck is reached, when coalescence becomes very rapid. Under this model, the coalescence date of island lineages 1 and 2 can be approximated by the formation of island 2 at time t2. In panel (b), population sizes are intermediate, and coalescence time is determined by the effective population size on the ancestral island.

Mentions: A second major source of uncertainty is the difference between the time at which two lineages cease interbreeding (which we assume is the colonization date) and the coalescence time of sequences sampled from those two species. Sequences sampled from sister species will be derived from different alleles in the ancestral population, and these alleles may have shared a common ancestor long before migration onto the new island occurred (Nei 1971, see illustration in fig. 1). This effect will be greatest when the effective population size is large, and the true coalescent time will lie between colonization of the donor island and migration onto the new island (fig. 1). Under a simple panmictic constant population model, the expected waiting time to coalescence for two alleles is 2 Ne generations, which for Drosophila is likely to be on the order of hundreds of thousands of years.Fig. 1.


Estimating divergence dates and substitution rates in the Drosophila phylogeny.

Obbard DJ, Maclennan J, Kim KW, Rambaut A, O'Grady PM, Jiggins FM - Mol. Biol. Evol. (2012)

Models linking speciation with coalescence. Panels (a–c) depict the coalescence of lineages (black lines) sampled at time t0 from three island-endemic species (labeled 1, 2, and 3). In this idealized model, speciation events can be associated with the colonization of island 2 from island 3 at time t2 and the colonization of island 1 from island 2 at time t1. Associating coalescence with speciation is less easy. In panel (a), population sizes are extremely small (depicted by the width of the gray background), so that coalescence happens extremely rapidly and the coalescence date of sequences sampled from islands 1 and 2 can be approximated to the date at which island 1 was colonized. In panel (c) within-island population sizes are effectively infinite, but the bottleneck at colonization is very tight. Thus, coalescence does not occur on the island until the colonization bottleneck is reached, when coalescence becomes very rapid. Under this model, the coalescence date of island lineages 1 and 2 can be approximated by the formation of island 2 at time t2. In panel (b), population sizes are intermediate, and coalescence time is determined by the effective population size on the ancestral island.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3472498&req=5

mss150-F1: Models linking speciation with coalescence. Panels (a–c) depict the coalescence of lineages (black lines) sampled at time t0 from three island-endemic species (labeled 1, 2, and 3). In this idealized model, speciation events can be associated with the colonization of island 2 from island 3 at time t2 and the colonization of island 1 from island 2 at time t1. Associating coalescence with speciation is less easy. In panel (a), population sizes are extremely small (depicted by the width of the gray background), so that coalescence happens extremely rapidly and the coalescence date of sequences sampled from islands 1 and 2 can be approximated to the date at which island 1 was colonized. In panel (c) within-island population sizes are effectively infinite, but the bottleneck at colonization is very tight. Thus, coalescence does not occur on the island until the colonization bottleneck is reached, when coalescence becomes very rapid. Under this model, the coalescence date of island lineages 1 and 2 can be approximated by the formation of island 2 at time t2. In panel (b), population sizes are intermediate, and coalescence time is determined by the effective population size on the ancestral island.
Mentions: A second major source of uncertainty is the difference between the time at which two lineages cease interbreeding (which we assume is the colonization date) and the coalescence time of sequences sampled from those two species. Sequences sampled from sister species will be derived from different alleles in the ancestral population, and these alleles may have shared a common ancestor long before migration onto the new island occurred (Nei 1971, see illustration in fig. 1). This effect will be greatest when the effective population size is large, and the true coalescent time will lie between colonization of the donor island and migration onto the new island (fig. 1). Under a simple panmictic constant population model, the expected waiting time to coalescence for two alleles is 2 Ne generations, which for Drosophila is likely to be on the order of hundreds of thousands of years.Fig. 1.

Bottom Line: Surprisingly, our estimate for the date for the most recent common ancestor of the genus Drosophila based on mutation rate (25-40 Ma) is closer to being compatible with independent fossil-derived dates (20-50 Ma) than are most of the Hawaiian-calibration models and also has smaller uncertainty.Potential problems with the Hawaiian calibration may arise from systematic variation in the molecular clock due to the long generation time of Hawaiian Drosophila compared with other Drosophila and/or uncertainty in linking island formation dates with colonization dates.As either source of error will bias estimates of divergence time, we suggest mutation rate estimates be used until better models are available.

View Article: PubMed Central - PubMed

Affiliation: Institute of Evolutionary Biology, and Centre for Infection Immunity and Evolution, University of Edinburgh, Edinburgh, United Kingdom. darren.obbard@ed.ac.uk

ABSTRACT
An absolute timescale for evolution is essential if we are to associate evolutionary phenomena, such as adaptation or speciation, with potential causes, such as geological activity or climatic change. Timescales in most phylogenetic studies use geologically dated fossils or phylogeographic events as calibration points, but more recently, it has also become possible to use experimentally derived estimates of the mutation rate as a proxy for substitution rates. The large radiation of drosophilid taxa endemic to the Hawaiian islands has provided multiple calibration points for the Drosophila phylogeny, thanks to the "conveyor belt" process by which this archipelago forms and is colonized by species. However, published date estimates for key nodes in the Drosophila phylogeny vary widely, and many are based on simplistic models of colonization and coalescence or on estimates of island age that are not current. In this study, we use new sequence data from seven species of Hawaiian Drosophila to examine a range of explicit coalescent models and estimate substitution rates. We use these rates, along with a published experimentally determined mutation rate, to date key events in drosophilid evolution. Surprisingly, our estimate for the date for the most recent common ancestor of the genus Drosophila based on mutation rate (25-40 Ma) is closer to being compatible with independent fossil-derived dates (20-50 Ma) than are most of the Hawaiian-calibration models and also has smaller uncertainty. We find that Hawaiian-calibrated dates are extremely sensitive to model choice and give rise to point estimates that range between 26 and 192 Ma, depending on the details of the model. Potential problems with the Hawaiian calibration may arise from systematic variation in the molecular clock due to the long generation time of Hawaiian Drosophila compared with other Drosophila and/or uncertainty in linking island formation dates with colonization dates. As either source of error will bias estimates of divergence time, we suggest mutation rate estimates be used until better models are available.

Show MeSH