A rich fossil record yields calibrated phylogeny for Acanthaceae (Lamiales) and evidence for marked biases in timing and directionality of intercontinental disjunctions

Syst Biol. 2014 Sep;63(5):660-84. doi: 10.1093/sysbio/syu029. Epub 2014 Apr 14.

Abstract

More than a decade of phylogenetic research has yielded a well-sampled, strongly supported hypothesis of relationships within the large ( > 4000 species) plant family Acanthaceae. This hypothesis points to intriguing biogeographic patterns and asymmetries in sister clade diversity but, absent a time-calibrated estimate for this evolutionary history, these patterns have remained unexplored. Here, we reconstruct divergence times within Acanthaceae using fossils as calibration points and experimenting with both fossil selection and effects of invoking a maximum age prior related to the origin of Eudicots. Contrary to earlier reports of a paucity of fossils of Lamiales (an order of ∼ 23,000 species that includes Acanthaceae) and to the expectation that a largely herbaceous to soft-wooded and tropical lineage would have few fossils, we recovered 51 reports of fossil Acanthaceae. Rigorous evaluation of these for accurate identification, quality of age assessment and utility in dating yielded eight fossils judged to merit inclusion in analyses. With nearly 10 kb of DNA sequence data, we used two sets of fossils as constraints to reconstruct divergence times. We demonstrate differences in age estimates depending on fossil selection and that enforcement of maximum age priors substantially alters estimated clade ages, especially in analyses that utilize a smaller rather than larger set of fossils. Our results suggest that long-distance dispersal events explain present-day distributions better than do Gondwanan or northern land bridge hypotheses. This biogeographical conclusion is for the most part robust to alternative calibration schemes. Our data support a minimum of 13 Old World (OW) to New World (NW) dispersal events but, intriguingly, only one in the reverse direction. Eleven of these 13 were among Acanthaceae s.s., which comprises > 90% of species diversity in the family. Remarkably, if minimum age estimates approximate true history, these 11 events occurred within the last ∼ 20 myr even though Acanthaceae s.s is over 3 times as old. A simulation study confirmed that these dispersal events were significantly skewed toward the present and not simply a chance occurrence. Finally, we review reports of fossils that have been assigned to Acanthaceae that are substantially older than the lower Cretaceous estimate for Angiosperms as a whole (i.e., the general consensus that has resulted from several recent dating and fossil-based studies in plants). This is the first study to reconstruct divergence times among clades of Acanthaceae and sets the stage for comparative evolutionary research in this and related families that have until now been thought to have extremely poor fossil resources.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Acanthaceae / classification*
  • Acanthaceae / genetics
  • DNA, Ribosomal Spacer / genetics
  • Fossils*
  • Genes, Plant / genetics
  • Phylogeny
  • Pollen / cytology
  • Time

Substances

  • DNA, Ribosomal Spacer