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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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Drosophila speciation on the Hawaiian Islands. As new Hawaiian islands are formed to the east, species from the nearest extant island are able to colonize the new island and become reproductively isolated (gray arrows). This "conveyer belt" speciation process has allowed the Hawaiian members of the Drosophilidae to radiate rapidly, forming a large and speciose group that display extreme morphological and behavioral diversity. This diversity includes the striking but now highly endangered "picture-wing" group (such as D. heteroneura, inset) that have been a major focus of Drosophila evolutionary ecology. The phylogeny (left) illustrates the inferred topology and speciation times of the seven species sampled for this study, with dates derived from model A1 (see main text), which sets speciation dates to the surface emergence of the first volcano of each island. Island dates are given as a span from the time of inferred surface emergence to shield completion for the oldest volcano on the island.
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mss150-F2: Drosophila speciation on the Hawaiian Islands. As new Hawaiian islands are formed to the east, species from the nearest extant island are able to colonize the new island and become reproductively isolated (gray arrows). This "conveyer belt" speciation process has allowed the Hawaiian members of the Drosophilidae to radiate rapidly, forming a large and speciose group that display extreme morphological and behavioral diversity. This diversity includes the striking but now highly endangered "picture-wing" group (such as D. heteroneura, inset) that have been a major focus of Drosophila evolutionary ecology. The phylogeny (left) illustrates the inferred topology and speciation times of the seven species sampled for this study, with dates derived from model A1 (see main text), which sets speciation dates to the surface emergence of the first volcano of each island. Island dates are given as a span from the time of inferred surface emergence to shield completion for the oldest volcano on the island.

Mentions: Coalescence in the ancestral population does not appear to have been explicitly modeled in previous studies of Hawaiian Drosophila, and some estimates have implicitly assumed the model illustrated in figure 1c, thus providing an upper limit on the age of speciation events. This model (fig. 1c) reflects a tight bottleneck at speciation causing rapid coalescence where local population sizes are otherwise extremely large (larger than continental populations of Drosophila) and thereby links between-species coalescence with the colonization of the ancestral island. For example, Bonacum et al. (2005) provided an upper limit for the MRCA of D. hemipeza and other species in the planitibia subgroup by associating the split with the formation of O‘ahu (2.6–3 Ma) and the split between D. differens/D. planitibia and D. silvestris/D. heteroneura with the formation of Moloka‘i (2 Ma). As D. hemipeza is endemic to O‘ahu and D. differens endemic to Moloka‘i (fig. 2), this model dates the divergence of the gene sequences as being over a million years before the species split. Although the widely cited studies of Russo et al. (1995) and Tamura et al. (2004) each used only used a single calibration date and chose to extrapolate over a much longer time frame, both also provided an upper-limit estimate by dating the MRCA of D. picticornis and the planitibia group by the formation of Kaua‘i (then estimated at 5.1 Ma), which is over a million years before the earliest possible speciation date (the formation of O‘ahu).Fig. 2.


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)

Drosophila speciation on the Hawaiian Islands. As new Hawaiian islands are formed to the east, species from the nearest extant island are able to colonize the new island and become reproductively isolated (gray arrows). This "conveyer belt" speciation process has allowed the Hawaiian members of the Drosophilidae to radiate rapidly, forming a large and speciose group that display extreme morphological and behavioral diversity. This diversity includes the striking but now highly endangered "picture-wing" group (such as D. heteroneura, inset) that have been a major focus of Drosophila evolutionary ecology. The phylogeny (left) illustrates the inferred topology and speciation times of the seven species sampled for this study, with dates derived from model A1 (see main text), which sets speciation dates to the surface emergence of the first volcano of each island. Island dates are given as a span from the time of inferred surface emergence to shield completion for the oldest volcano on the island.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

mss150-F2: Drosophila speciation on the Hawaiian Islands. As new Hawaiian islands are formed to the east, species from the nearest extant island are able to colonize the new island and become reproductively isolated (gray arrows). This "conveyer belt" speciation process has allowed the Hawaiian members of the Drosophilidae to radiate rapidly, forming a large and speciose group that display extreme morphological and behavioral diversity. This diversity includes the striking but now highly endangered "picture-wing" group (such as D. heteroneura, inset) that have been a major focus of Drosophila evolutionary ecology. The phylogeny (left) illustrates the inferred topology and speciation times of the seven species sampled for this study, with dates derived from model A1 (see main text), which sets speciation dates to the surface emergence of the first volcano of each island. Island dates are given as a span from the time of inferred surface emergence to shield completion for the oldest volcano on the island.
Mentions: Coalescence in the ancestral population does not appear to have been explicitly modeled in previous studies of Hawaiian Drosophila, and some estimates have implicitly assumed the model illustrated in figure 1c, thus providing an upper limit on the age of speciation events. This model (fig. 1c) reflects a tight bottleneck at speciation causing rapid coalescence where local population sizes are otherwise extremely large (larger than continental populations of Drosophila) and thereby links between-species coalescence with the colonization of the ancestral island. For example, Bonacum et al. (2005) provided an upper limit for the MRCA of D. hemipeza and other species in the planitibia subgroup by associating the split with the formation of O‘ahu (2.6–3 Ma) and the split between D. differens/D. planitibia and D. silvestris/D. heteroneura with the formation of Moloka‘i (2 Ma). As D. hemipeza is endemic to O‘ahu and D. differens endemic to Moloka‘i (fig. 2), this model dates the divergence of the gene sequences as being over a million years before the species split. Although the widely cited studies of Russo et al. (1995) and Tamura et al. (2004) each used only used a single calibration date and chose to extrapolate over a much longer time frame, both also provided an upper-limit estimate by dating the MRCA of D. picticornis and the planitibia group by the formation of Kaua‘i (then estimated at 5.1 Ma), which is over a million years before the earliest possible speciation date (the formation of O‘ahu).Fig. 2.

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