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Comparative Study
. 2005 Jul 22;272(1571):1481-90.
doi: 10.1098/rspb.2005.3067.

Repeated evolution of net venation and fleshy fruits among monocots in shaded habitats confirms a priori predictions: evidence from an ndhF phylogeny

Thomas J Givnish  1 , J Chris Pires, Sean W Graham, Marc A McPherson, Linda M Prince, Thomas B Patterson, Hardeep S Rai, Eric H Roalson, Timothy M Evans, William J Hahn, Kendra C Millam, Alan W Meerow, Mia Molvray, Paul J Kores, Heath E O'Brien, Jocelyn C Hall, W John Kress, Kenneth J Sytsma
Affiliations
Comparative Study

Repeated evolution of net venation and fleshy fruits among monocots in shaded habitats confirms a priori predictions: evidence from an ndhF phylogeny

Thomas J Givnish et al. Proc Biol Sci. .

Abstract

We present a well-resolved, highly inclusive phylogeny for monocots, based on ndhF sequence variation, and use it to test a priori hypotheses that net venation and vertebrate-dispersed fleshy fruits should undergo concerted convergence, representing independent but often concurrent adaptations to shaded conditions. Our data demonstrate that net venation arose at least 26 times and was lost eight times over the past 90 million years; fleshy fruits arose at least 21 times and disappeared 11 times. Both traits show a highly significant pattern of concerted convergence (p<10(-9)), arising 16 times and disappearing four times in tandem. This phenomenon appears driven by even stronger tendencies for both traits to evolve in shade and be lost in open habitats (p<10(-13)-10(-29)). These patterns are among the strongest ever demonstrated for evolutionary convergence in individual traits and the predictability of evolution, and the strongest evidence yet uncovered for concerted convergence. The rate of adaptive shifts per taxon has declined exponentially over the past 90 million years, as expected when large-scale radiations fill adaptive zones.

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Figures

Figure 1
Figure 1
A phylogram of one of 874 most-parsimonious trees produced by a maximum-parsimony analysis of ndhF sequence variation. Branch lengths are proportional to the number of mutations inferred down each lineage. Arrowheads indicate nodes that collapse in the strict consensus tree; bootstrap values (orders and commelinids only) are indicated above each node. See Electronic Appendix for bootstrap values at other nodes.
Figure 2
Figure 2
Concerted convergence of net venation (green), fleshy fruits (red), shaded habitats (sand boxes) and broad-leaved aquatic habitats (blue boxes). Note that almost all transitions to net venation and fleshy fruits occur upon invasion of shaded habitats, and that almost all reversals to parallel venation and dry, passively dispersed seeds or fruits occur upon re-invasion of open, sunny habitats. Branching has been calibrated against time based on fossil data, so that the tempo and taxonomic distribution of phenotypic transitions can be visualized.
Figure 3
Figure 3
Rate of adaptive transitions in venation and fruit characters (gains and losses per clade per 10 Myr) in the monocots over the past 90 Myr. The rate of such transitions was highest early in monocot evolution and subsequently dropped exponentially with time (y=0.052 e−0.018x; r2=0.78, p<0.001 for 7 d.f.). Dashed curve represents the regression without data for the earliest interval (outlier for mean, variance) included. This analysis underestimates the decline in the rate of adaptive change, because our sample (ca. 0.5% of all monocot species) is biased towards including families and groups in which net venation and fleshy fruits have evolved, and away from the most recent, phenotypically repetitive diversification within families and genera. Inclusion of the latter would greater inflate the number of recent clades and add few new shifts in venation or fruit type.
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