Age and rate of diversification of the Hawaiian silversword alliance (Compositae)

Abstract

Comparisons between insular and continental radiations have been hindered by a lack of reliable estimates of absolute diversification rates in island lineages. We took advantage of rate-constant rDNA sequence evolution and an ''external'' calibration using paleoclimatic and fossil data to determine the maximum age and minimum diversification rate of the Hawaiian silversword alliance (Compositae), a textbook example of insular adaptive radiation in plants.Our maximum-age estimate of 5.2 ؎ 0.8 million years ago for the most recent common ancestor of the silversword alliance is much younger than ages calculated by other means for the Hawaiian drosophilids, lobelioids, and honeycreepers and falls approximately within the history of the modern high islands (<5.1 ؎ 0.2 million years ago). By using a statistically efficient estimator that reduces error variance by incorporating clock-based estimates of divergence times, a minimum diversification rate for the silversword alliance was estimated to be 0.56 ؎ 0.17 species per million years. This exceeds average rates of more ancient continental radiations and is comparable to peak rates in taxa with sufficiently rich fossil records that changes in diversification rate can be reconstructed.The Hawaiian silversword alliance (Argyroxiphium, Dubautia, Wilkesia; Compositae) has been considered ''the best example of adaptive radiation in plants'' (1). Life-form diversity among the 28 Hawaiian-endemic species in the group encompasses trees, shrubs, subshrubs, mat-plants, monocarpic and polycarpic rosette plants, cushion plants, and vines that occur across a broad environmental spectrum, from rainforests to desert-like settings (2). Although monophyly of the group is well established (3), absolute ages of the silversword alliance and other Hawaiian lineages have been difficult to estimate. Ages are essential in the reconstruction of the absolute diversification rates-the rate of speciation minus extinction (S Ϫ E). Availability of such rate estimates would permit comparisons with other insular radiations and with continental radiations, which may exhibit qualitatively or quantitatively different patterns of diversification.Unfortunately, knowledge of island ages from potassiumargon dating is of minimal value for placing upper limits on ages of lineages in ancient hot-spot archipelagos such as the Hawaiian Islands. The age of terrestrial groups in the Hawaiian archipelago can conceivably date back to the formation of Kure [29 million years ago (Ma)], under the assumption of an unbroken succession of dispersals from older to younger islands since that time (4). An upper age limit of 29 Ma is too high to be of any value for dating island radiations in groups such as Asteraceae-the oldest unequivocal fossil evidence of the family worldwide is more recent, from the mid-Oligocene (5). Moreover, calibration of clock-like divergence of molecular sequences is complicated if individual island ages are used to estimate the age of an entire insular radiation (''internal'' calibration)...

The quest to resolve recent radiations: Plastid phylogenomics of extinct and endangered Hawaiian endemic mints (Lamiaceae)

“…Phylogenies of the Hawaiian mints have been reconstructed from datasets composed of commonly used DNA sequence markers, including cpDNA and nuclear ribosomal 5S non-transcribed spacer and external transcribed spacer regions (Lindqvist and Albert, 2002;Roy et al, 2013), which are rapidly evolving in many other species (Baldwin and Markos, 1998;Shaw et al, 2005;Small et al, 1998), but they fail to resolve relationships among the Hawaiian mints. A similar pattern of low genetic diversity has been noted in other recent radiations of Hawaiian plants (Appelhans et al, 2014;Baldwin and Sanderson, 1998;Cronk et al, 2005;Givnish et al, 2009;Givnish et al, 2013). Given this low diversity in recent radiations, large amounts of data are clearly required to increase resolution.…”

Δ6-Desaturase sequence evidence for explosive Pliocene radiations within the adaptive radiation of Macaronesian Echium (Boraginaceae)

“…Our analysis demonstrates that the circularity of using morphological characters subject to selection can lead misinterpretations of sectional taxonomy and species relationships (Bramwell, 1972(Bramwell, , 1973(Bramwell, , 1975 (Fig. 2), particularly in the accelerated change occurring on oceanic islands (Givnish and Sytsma, 1997;Baldwin and Sanderson, 1998). Simpson (1953) added a new twist to the definition of adaptive radiation by introducing a temporal scale.…”

“…Trees were then described with gamma-distributed rate variation and four rate categories were assumed. Differences in the log-likelihoods of clock-constrained and clockunconstrained trees were assessed for statistical significance following the logic of Baldwin and Sanderson (1998). To infer divergence times, we used tree topology and branch lengths obtained from the ML results.…”

Pattern and timing of diversification in Yucca (Agavaceae): specialized pollination does not escalate rates of diversification

“…Divergence times and mutation rates were estimated using penalized likelihood in r8s v. 1.71 (Sanderson 1997(Sanderson , 2002. Relative and absolute speciation rates were compared between Yucca and its sister group (Agave sensu latissimus) using a randomly branching Markovian model (Slowinski & Guyer 1989), a likelihood ratio test (Sanderson & Donoghue 1994), a Yule model (Baldwin & Sanderson 1998), and lineages-through-time plots, calculting Phybus's gamma statistic (Pybus et al 2002). Detailed descriptions of the laboratory and analytical methods are available as electronic supplementary material.…”