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Exploring the ontogenetic scaling hypothesis during the diversification of pollination syndromes in Caiophora (Loasaceae, subfam. Loasoideae).

ABSTRACT: Phenotypic diversification of flowers is frequently attributed to selection by different functional groups of pollinators. During optimization of floral phenotype, developmental robustness to genetic and non-genetic perturbations is expected to limit the phenotypic space available for future evolutionary changes. Although adaptive divergence can occur without altering the basic developmental programme of the flower (ontogenetic scaling hypothesis), the rarity of reversion to ancestral states following adaptive radiations of pollination syndromes suggests that changes in the ancestral developmental programme of the flower are common during such evolutionary transitions. Evidence suggests that flower diversification into different pollination syndromes in the Loasoideae genus Caiophora took place during a recent adaptive radiation in the central Andes. This involved transitions from bee to hummingbird and small rodent pollination. The aim of this work was to examine if the adaptive radiation of pollination syndromes in Caiophora occurred through ontogenetic scaling or involved a departure from the ontogenetic pattern basal to this genus.We used geometric morphometric variables to describe the shape and size of floral structures taking part in the pollination mechanism of Loasoideae. This approach was used to characterize the developmental trajectories of three species basal to the genus Caiophora through shape-size relationships (ontogenetic allometry). We then tested if the shape-size combinations of these structures in mature flowers of derived Caiophora species fall within the phenotypic space predicted by the development of basal species.Variation in the size and shape of Caiophora flowers does not overlap with the pattern of ontogenetic allometry of basal species. Derived bee-, hummingbird- and rodent-pollinated species had divergent ontogenetic patterns of floral development from that observed for basal bee-pollinated species.The adaptive radiation of Caiophora involved significant changes in the developmental pattern of the flowers, rejecting the ontogenetic scaling hypothesis.

SUBMITTER: Strelin MM

PROVIDER: S-EPMC4845809 | biostudies-other | 2016 Apr

REPOSITORIES: biostudies-other

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Exploring the ontogenetic scaling hypothesis during the diversification of pollination syndromes in Caiophora (Loasaceae, subfam. Loasoideae).

Strelin Marina M MM Benitez-Vieyra Santiago S Fornoni Juan J Klingenberg Christian Peter CP Cocucci Andrea A AA

Annals of botany. 20160406 5

<h4>Background and aims</h4>Phenotypic diversification of flowers is frequently attributed to selection by different functional groups of pollinators. During optimization of floral phenotype, developmental robustness to genetic and non-genetic perturbations is expected to limit the phenotypic space available for future evolutionary changes. Although adaptive divergence can occur without altering the basic developmental programme of the flower (ontogenetic scaling hypothesis), the rarity of rever ...[more]

PMID: 27056974

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Project description:Background and aimsSimple models of herbaceous plant growth based on optimal partitioning theory predict, at steady state, an isometric relationship between shoot and root biomass during plant ontogeny, i.e. a constant root-shoot ratio. This prediction has received mixed empirical support, suggesting either that optimal partitioning is too coarse an assumption to model plant biomass allocation, or that additional processes need to be modelled to account for empirical findings within the optimal partitioning framework. In this study, simulations are used to compare quantitatively two potential explanations for observed non-isometric relationships, namely nutrient limitation during the experiments and initial developmental constraints.MethodsA simple plant growth model was built to simulate the growth of herbaceous species, based on optimal partitioning theory combined with empirically measured plant functional traits. Its ability to reproduce plant relative growth rate and final root weight ratio was assessed against previously published data. Predicted root-shoot ratios during plant ontogeny were compared with experimental observations. The effects of nutrient limitation and initial developmental constraints on root-shoot ratios were then tested.Key resultsThe model was found to reproduce overall plant growth patterns accurately, but failed, in its simplest form, at explaining non-isometric growth trajectories. Both nutrient limitation and ontogenetic developmental constraints were further shown to cause transient dynamics resulting in a deviation from isometry. Nitrogen limitation alone was not sufficient to explain the observed trajectories of most plant species. The inclusion of initial developmental constraints (fixed non-optimal initial root-shoot ratios) enabled the reproduction of the observed trajectories and were consistent with observed initial root-shoot ratios.ConclusionsThis study highlights the fact that considering transient dynamics enables theoretical predictions based on optimal partitioning to be reconciled with empirically measured ontogenetic root-shoot allometries. The transient dynamics cannot be solely explained by nutrient limitation during the experiments, pointing to a likely role for initial developmental constraints in the observed non-isometric growth trajectories.

Project description:A striking characteristic of the Western North American flora is the repeated evolution of hummingbird pollination from insect-pollinated ancestors. This pattern has received extensive attention as an opportunity to study repeated trait evolution as well as potential constraints on evolutionary reversibility, with little attention focused on the impact of these transitions on species diversification rates. Yet traits conferring adaptation to divergent pollinators potentially impact speciation and extinction rates, because pollinators facilitate plant reproduction and specify mating patterns between flowering plants. Here, we examine macroevolutionary processes affecting floral pollination syndrome diversity in the largest North American genus of flowering plants, Penstemon. Within Penstemon, transitions from ancestral bee-adapted flowers to hummingbird-adapted flowers have frequently occurred, although hummingbird-adapted species are rare overall within the genus. We inferred macroevolutionary transition and state-dependent diversification rates and found that transitions from ancestral bee-adapted flowers to hummingbird-adapted flowers are associated with reduced net diversification rate, a finding based on an estimated 17 origins of hummingbird pollination in our sample. Although this finding is congruent with hypotheses that hummingbird adaptation in North American Flora is associated with reduced species diversification rates, it contrasts with studies of neotropical plant families where hummingbird pollination has been associated with increased species diversification. We further used the estimated macroevolutionary rates to predict the expected pattern of floral diversity within Penstemon over time, assuming stable diversification and transition rates. Under these assumptions, we find that hummingbird-adapted species are expected to remain rare due to their reduced diversification rates. In fact, current floral diversity in the sampled Penstemon lineage, where less than one-fifth of species are hummingbird adapted, is consistent with predicted levels of diversity under stable macroevolutionary rates.

Dataset Information

Exploring the ontogenetic scaling hypothesis during the diversification of pollination syndromes in Caiophora (Loasaceae, subfam. Loasoideae).

Publications

Exploring the ontogenetic scaling hypothesis during the diversification of pollination syndromes in Caiophora (Loasaceae, subfam. Loasoideae).

Similar Datasets

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