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Evolution of a Hotspot Genus: Geographic Variation in Speciation and Extinction Rates in Banksia (Proteaceae)

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Evolution of a Hotspot Genus: Geographic Variation in Speciation and Extinction Rates in Banksia (Proteaceae)

Marcel Cardillo et al. BMC Evol Biol.

Abstract

Background: Hotspots of angiosperm species richness and endemism in Mediterranean-climate regions are among the most striking, but least well-understood, geographic patterns of biodiversity. Recent studies have emphasized the importance of rapid diversification within hotspots, compared to non-hotspot regions, as a major contributor to these patterns. We constructed the first near-complete phylogeny of Banksia (Proteaceae) to test whether diversification rates have differed between lineages confined to the southwest Australian hotspot and those found throughout southern, eastern and northern Australia. We then tested for variation in diversification rates among the bioclimatic zones within the southwest hotspot itself.

Results: Although Banksia species richness in the southwest is ten times that of the rest of the continent, we find little evidence for more rapid diversification in the southwest, although this result is inconclusive. However, we find firmer support for substantial rate variation within the southwest hotspot, with more rapid diversification in the semi-arid heaths and shrublands, compared to the high-rainfall forests. Most of the Banksia diversity of the southwest appears to be generated in the heaths and shrublands, with a high migration rate out of this zone boosting diversity of the adjacent forest zone.

Conclusions: The geographic pattern of diversification in Banksia appears more complex than can be characterized by a simple hotspot vs. non-hotspot comparison, but in general, these findings contrast with the view that the high diversity of Mediterranean hotspots is underpinned by rapid radiations. Steady accumulation of species at unexceptional rates, but over long periods of time, may also have contributed substantially to the great botanical richness of these regions.

Figures

Figure 1
Figure 1
Map of Australia showing the distribution of Banksia. The overall distribution of the genus is approximated by the locations of origin of herbarium specimens (orange squares). The areas outlined in blue are the transitional rainfall zone and south coast province (TRZ + SCP), and the high rainfall zone (HRZ), which together form the Southwest Botanical Province.
Figure 2
Figure 2
Maximum clade credibility tree of Banksia from a BEAST analysis. Coloured symbols at the tips indicate geographic distributions: orange = non-SWBP; red = TRZ + SCP; blue = HRZ; green = both TRZ + SCP and HRZ. The black square indicates the crown node of the Dryandra clade. Timescale is in millions of years bp.
Figure 3
Figure 3
Temporal patterns of Banksia diversification. (a) Accumulation of lineages through time for a sample of 250 Banksia phylogenies from the Bayesian posterior distribution. The solid line connects the median divergence times for each number of lineages. (b) Distribution of values of the gamma statistic for the 250 phylogenies.
Figure 4
Figure 4
Regressions of crown age against clade size. For each of 250 Banksia phylogenies sampled from the Bayesian posterior distribution, a set of independent clades was identified by counting six nodes down from the root. Regressions were fitted across these clades, giving 250 slope estimates. The open circles and bars represent the median and HPD of the crown age estimates for the two non-SWBP Banksia clades.
Figure 5
Figure 5
Distributions of BiSSE parameter estimates. The panels show distributions of estimates of (a,b) speciation rates, (c,d) extinction rates, and (e,f) diversification rates, for 250 phylogenies from the Bayesian posterior distribution, from a BiSSE analysis in which all parameters were free to vary (the full model). Upper and lower panels are estimates for non-SWBP and SWBP clades, respectively.
Figure 6
Figure 6
BiSSE model comparisons. The panels show ∆AIC values for 250 phylogenies from the Bayesian posterior distribution. (a) Equal-rates vs full model; (b) Equal-rates vs equal-speciation model; (c) equal-rates vs equal-extinction model.
Figure 7
Figure 7
Distributions of GeoSSE parameter estimates. The panels show distributions of estimates of (a,b) speciation rates, (c,d) extinction rates, (e,f) diversification rates, and (g,h) migration rates, for 250 phylogenies from the Bayesian posterior distribution, from a GeoSSE analysis in which all parameters were free to vary (the full model). Upper and lower panels are estimates for HRZ and TRZ + SCP species, respectively.
Figure 8
Figure 8
GeoSSE model comparisons. The panels show ∆AIC values for 250 phylogenies from the Bayesian posterior distribution. (a) Equal-rates vs full model; (b) Equal-rates vs equal-speciation model; (c) equal-rates vs equal-extinction model; (d) equal-rates vs equal-dispersal model.

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