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. 2008 Aug;102(2):153-65.
doi: 10.1093/aob/mcn082. Epub 2008 May 28.

Evolutionary Trends in the Flowers of Asteridae: Is Polyandry an Alternative to Zygomorphy?

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Evolutionary Trends in the Flowers of Asteridae: Is Polyandry an Alternative to Zygomorphy?

Florian Jabbour et al. Ann Bot. .
Free PMC article

Abstract

Background and aims: Floral symmetry presents two main states in angiosperms, actinomorphy (polysymmetry or radial symmetry) and zygomorphy (monosymmetry or bilateral symmetry). Transitions from actinomorphy to zygomorphy have occurred repeatedly among flowering plants, possibly in coadaptation with specialized pollinators. In this paper, the rules controlling the evolution of floral symmetry were investigated to determine in which architectural context zygomorphy can evolve.

Methods: Floral traits potentially associated with perianth symmetry shifts in Asteridae, one of the major clades of the core eudicots, were selected: namely the perianth merism, the presence and number of spurs, and the androecium organ number. The evolution of these characters was optimized on a composite tree. Correlations between symmetry and the other morphological traits were then examined using a phylogenetic comparative method.

Key results: The analyses reveal that the evolution of floral symmetry in Asteridae is conditioned by both androecium organ number and perianth merism and that zygomorphy is a prerequisite to the emergence of spurs.

Conclusions: The statistically significant correlation between perianth zygomorphy and oligandry suggests that the evolution of floral symmetry could be canalized by developmental or spatial constraint. Interestingly, the evolution of polyandry in an actinomorphic context appears as an alternative evolutionary pathway to zygomorphy in Asteridae. These results may be interpreted either in terms of plant-pollinator adaptation or in terms of developmental or physical constraints. The results are discussed in relation to current knowledge about the molecular bases underlying floral symmetry.

Figures

F<sc>ig</sc>. 1.
Fig. 1.
Composite tree of the Asteridae where the evolution of perianth merism is optimized using the maximum parsimony method. Branches are coloured according to the observed (terminal branches) and inferred (internal branches) character state. Yellow, Trimery/hexamery; red, tetramery; blue, pentamery; green, heptamery; grey, variable; black, undefined. The orders indicated on the right-hand side of the tree are according to the classification of APG (2003). Taxon names are in the same order as the leaves of the tree from top to bottom and are coloured according to the order to which they belong.
F<sc>ig</sc>. 2.
Fig. 2.
Mirror trees of the Asteridae showing the evolution of perianth symmetry and androecium organ number optimized using maximum parsimony. (A) Evolution of perianth symmetry. Black, Actinomorphy; red, zygomorphy. (B) Evolution of androecium organ number. Black, Oligandry (≤2 times the ancestral perianth merism); red, polyandry (>2 times the ancestral perianth merism). Coloured lines and numbers refer to the orders of Asteridae as in Fig. 1. 1, Garryales; 2, Untitled Group 1; 3, Gentianales; 4, Solanales; 5, Lamiales; 6, Aquifoliales; 7, Apiales; 8, Dipsacales; 9, Untitled Group 2; 10, Asterales; 11, Ericales; 12, Cornales.
F<sc>ig</sc>. 3.
Fig. 3.
Mirror trees of the Asteridae showing the evolution of perianth symmetry and the number of spurs optimized using the maximum parsimony method. (A) Evolution of perianth symmetry. Black, Actinomorphy; red, zygomorphy. (B) Evolution of the number of spurs. Black, 0 or equal to perianth merism; red, inferior to perianth merism. Coloured lines and numbers refer to the orders of Asteridae as in Fig. 1. 1, Garryales; 2, Untitled Group 1; 3, Gentianales; 4, Solanales; 5, Lamiales; 6, Aquifoliales; 7, Apiales; 8, Dipsacales; 9, Untitled Group 2; 10, Asterales; 11, Ericales; 12, Cornales.
F<sc>ig</sc>. 4.
Fig. 4.
Flow diagram summarizing the transitions between the different states of androecium organ number and perianth symmetry. Parameter qij is the transition rate between state ‘i’ in androecium organ number and state ‘j’ in perianth symmetry. Only the transition rates that are significantly different from zero are shown [q12, q21, q13, q31, q43 ≠ 0 (P < 0·05)]. Transition q31 (thick arrow) has a significantly higher value than transition q13 (thin arrow; P < 0·001), idem for q43 and q21 (P < 0·05). q21 and q12 are not significantly different (P = 0·180), the same for q12 and q13 (P = 0·067).
F<sc>ig</sc>. 5.
Fig. 5.
Proposed scenario for the evolution of perianth symmetry and related characters in Asteridae. The characters are, from top to bottom, perianth symmetry, androecium organ number, the number of spurs, perianth merism. New acquisitions (derived states) are underlined and in bold. A single circle in a grey ellipse indicates association of states ‘zygomorphy + oligandry’. Two circles in a grey ellipse indicates association of states ‘zygomorphy + polyandry’.
F<sc>ig</sc>. 6.
Fig. 6.
Proposed stability diagram of the ‘perianth symmetry + androecium organ number’ states. The ‘actinomorphic + oligandrous’ (A, <) state is the most stable (square), whereas the ‘zygomorphic + polyandrous’, ‘actinomorphic + polyandrous’ (A, >), and ‘zygomorphic + oligandrous’ (Z, <) are unstable states (circles). Climbing over a ‘hill’ of morphogenetic cost is less probable than reverting to the ancestral state. The height of the ‘hills’ (Z, >), (A, >) and (Z, <) are proportional to the differences q43q34, q31q13 and q21q12.

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