Evolution of Plant Architecture, Functional Diversification and Divergent Evolution in the Genus Atractocarpus (Rubiaceae) for New Caledonia

Abstract

The diversification of ecological roles and related adaptations in closely related species within a lineage is one of the most important processes linking plant evolution and ecology. Plant architecture offers a robust framework to study these processes as it can highlight how plant structure influences plant diversification and ecological strategies. We investigated a case of gradual evolution of branching architecture in Atractocarpus spp. (Rubiaceae), forming a monophyletic group in New Caledonia that has diversified rapidly, predominantly in rainforest understory habitats. We used a transdisciplinary approach to depict architectural variations and revealed multiple evolutionary transitions from a branched (Stone's architectural model) to a monocaulous habit (Corner's architectural model), which involved the functional reduction of branches into inflorescences. We propose an integrative functional index that assesses branching incidence on functional traits influencing both assimilation and exploration functions. We showed that architectural transitions correlate with ecologically important functional traits. Variation in ecologically important traits among closely relatives, as supported by the architectural analysis, is suggestive of intense competition that favored divergence among locally coexisting species. We propose that Pleistocene climatic fluctuations causing expansion and contraction of rainforest could also have offered ecological opportunities for colonizers in addition to the process of divergent evolution.

Keywords: Island; branching index; convergence; corner's rules; gardenieae; rainforest; treelet; understory.

Figure 1

Photographs of different Atractocarpus species in their environment showing variability in growth habit and lateral axis. Monocaulous species: (A) A. confertus, (B) A. bracteatus, (C) A. bracteatus. Intermediate species: (D) A. ngoyensis, (E) A. ngoyensis, (F) A. ngoyensis. Branched species: (G) A. pseudoterminalis, (H) A. sp. nov. 10, (I) A. pseudoterminalis.

Figure 2

Branching indexes calculated on the base of (A) exploration function, (B) photosynthetic function and (C) the combination of both, for 25 Atractocarpus species. Letters in (C) correspond to the result of the Wilcoxon test; species with shared letters are not significantly different for a given risk of error.

Figure 3

Schematic representation of the three main architectural classes found in the rainforest understory species of Atractocarpus: (A) Monocaulous, (B) Intermediate (C) Branched.

Figure 4

Photographs of branches with their axillary leaves (i.e., from trunk) for height Atractocarpus species with different branching degrees. Arrows indicate apical death, i.e., flowering sites (for A. longistipitatus (E), only half of apical death has been represented). Branched species: (A) A. pseudoterminalis, (B) A. sp4. Intermediate species: (C) A. ngoyensis, (D) A. brandzeanus. Monocaulous species: (E) A. longistipitatus, (F) A. pterocarpon, (G) A. bracteatus, (H) A. confertus.

Figure 5

Projection of (A) species and (B) traits on the two first axis of Principal Component Analysis (see Table 1 for trait abbreviations). Ellipses represent the 95% confidence interval for each architectural classes. Functional differences between architectural classes were tested with Permanova.

Figure 6

Estimation of ancestral architectural class in the genus Atractocarpus. Numbers correspond to the Bayesian probability for each reconstituted node. Gray box highlights New Caledonian clade. Letters (A, B) highlight major clades were shifts from branched to monocaulous or intermediate architecture operate.