Morphological and molecular phylogenetic context of the angiosperms: contrasting the “top down” and “bottom-up” approaches to inferring the likely characteristics of the first flowers

RM Bateman, Jason Hilton, PJ Rudall

Research output: Contribution to journalArticle

107 Citations (Scopus)

Abstract

Recent attempts to address the long-debated 'origin' of the angiosperms depend on a phylogenetic framework derived from a matrix of taxa versus characters; most assume that empirical rigour is proportional to the size of the matrix. Sequence-based genotypic approaches increase the number of characters (nucleotides and indels) in the matrix but are confined to the highly restricted spectrum of extant species, whereas morphology-based approaches increase the number of phylogenetically informative taxa (including fossils) at the expense of accessing only a restricted spectrum of phenotypic characters. The two approaches are currently delivering strongly contrasting hypotheses of relationship. Most molecular studies indicate that all extant gymnosperms form a natural group, suggesting surprisingly early divergence of the lineage that led to angiosperms, whereas morphology-only phylogenies indicate that a succession of (mostly extinct) gymnosperms preceded a later angiosperm origin. Causes of this conflict include: (1) the vast phenotypic and genotypic lacuna, largely reflecting pre-Cenozoic extinctions, that separates early-divergent living angiosperms from their closest relatives among the living gymnosperms; (ii) profound uncertainty regarding which (a) extant and (b) extinct angiosperms are most closely related to gymnosperms; and (iii) profound uncertainty regarding which (a) extant and (b) extinct gymnosperms are most closely related to angiosperms, and thus best serve as 'outgroups' dictating the perceived evolutionary polarity of character transitions among the early-divergent angiosperms. These factors still permit a remarkable range of contrasting, yet credible, hypotheses regarding the order of acquisition of the many phenotypic characters, reproductive and vegetative, that distinguish 'classic' angiospermy from 'classic' gymnospermy. The flower remains ill-defined and its mode (or modes) of origin remains hotly disputed; some definitions and hypotheses of evolutionary relationships preclude a role for the flower in delimiting the angiosperms. We advocate maintenance of parallel, reciprocally illuminating programmes of morphological and molecular phylogeny reconstruction, respectively supported by homology testing through additional taxa (especially fossils) and evolutionary-developmental genetic studies that explore genes potentially responsible for major phenotypic transitions.
Original languageEnglish
Pages (from-to)3471-3503
Number of pages33
JournalJournal of Experimental Botany
Volume57
DOIs
Publication statusPublished - 15 Sept 2006

Keywords

  • congruence
  • tree rooting
  • development
  • evolutionary-developmental genetics
  • phylogeny
  • outgroup
  • angiosperm
  • gene duplication
  • morphology
  • gymnosperm
  • pteridophyte
  • ontogeny
  • fossil
  • taxon sampling
  • character optimization
  • flower

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