skip to main content


Title: Remarkable variation in androecial morphology is closely associated with corolla traits in Western Hemisphere Justiciinae (Acanthaceae: Justicieae)
Abstract Background and Aims

Few studies of angiosperms have focused on androecial evolution in conjunction with evolutionary shifts in corolla morphology and pollinator relationships. The Western Hemisphere clade of Justiciinae (Acanthaceae) presents the rare opportunity to examine remarkable diversity in staminal morphology. We took a phylogenetically informed approach to examine staminal diversity in this hypervariable group and asked whether differences in anther thecae separation is associated with phylogenetically informed patterns of variation in corolla morphology. We further discuss evidence for associations between anther diversity and pollinators in this lineage.

Methods

For the Dianthera/Sarotheca/Plagiacanthus (DSP) clade of Western Hemisphere Justiciinae, we characterized floral diversity based on a series of corolla measurements and using a model-based clustering approach. We then tested for correlations between anther thecae separation and corolla traits, and for shifts in trait evolution, including evidence for convergence.

Key Results

There is evolutionary vagility in corolla and anther traits across the DSP clade with little signal of phylogenetic constraint. Floral morphology clusters into four distinct groups that are, in turn, strongly associated with anther thecae separation, a novel result in Acanthaceae and, to our knowledge, across flowering plants. These cluster groups are marked by floral traits that strongly point to associations with pollinating animals. Specifically, species that are known or likely to be hummingbird pollinated have stamens with parallel thecae, whereas those that are likely bee or fly pollinated have stamens with offset, divergent thecae.

Conclusions

Our results suggest that anther thecae separation is likely under selection in concert with other corolla characters. Significant morphological shifts detected by our analyses corresponded to putative shifts from insect to hummingbird pollination. Results from this study support the hypothesis that floral structures function in an integrated manner and are likely subject to selection as a suite. Further, these changes can be hypothesized to represent adaptive evolution.

 
more » « less
NSF-PAR ID:
10467635
Author(s) / Creator(s):
; ; ; ;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
Annals of Botany
Volume:
132
Issue:
1
ISSN:
0305-7364
Format(s):
Medium: X Size: p. 43-60
Size(s):
["p. 43-60"]
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract A fundamental question in evolutionary biology is how clades of organisms exert influence on one another. The evolution of the flower and subsequent plant/pollinator coevolution are major innovations that have operated in flowering plants to promote species radiations at a variety of taxonomic levels in the Neotropics. Here we test the hypothesis that pollination by Neotropical endemic hummingbirds drove the evolution of two unique stigma traits in correlation with other floral traits in New World Salvia (Lamiaceae). We examined morphometric shapes of stigma lobing across 400 Salvia spp., scored presence and absence of a stigma brush across Salvia, and used a suite of phylogenetic comparative methods to detect shape regime shifts, correlation of trait shifts with BayesTraits and phylogenetic generalized least square regressions, and the influence of scored pollinators on trait evolution using OUwie. We found that a major Neotropical clade of Salvia evolved a correlated set of stigma features, with a longer upper stigma lobe and stigmatic brush, following an early shift to hummingbird pollination. Evolutionary constraint is evident as subsequent shifts to bee pollination largely retained these two features. Our results support the hypothesis that hummingbirds guided the correlative shifts in corolla, anther connective, style and stigma shape in Neotropical Salvia, despite repeated shifts back to bee pollination. 
    more » « less
  2. Abstract

    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.

     
    more » « less
  3. Abstract

    Fusion of petals to form a corolla tube is considered a key innovation contributing to the diversification of many flowering plant lineages. Corolla tube length often varies dramatically among species and is a major determinant of pollinator preference. However, our understanding of the developmental dynamics underlying corolla tube length variation is very limited. Here we examined corolla tube growth in theMimulus lewisiispecies complex, an emerging model system for studying the developmental genetics and evo‐devo of pollinator‐associated floral traits. We compared developmental and cellular processes associated with corolla tube length variation among the bee‐pollinatedM. lewisii, the hummingbird‐pollinatedMimulus verbenaceus, and the self‐pollinatedMimulus parishii. We found that in all three species, cell size is non‐uniformly distributed along the mature tube, with the longest cells just distal to the stamen insertion site. Differences in corolla tube length among the three species are not associated with processes of organogenesis or early development but are associated with variation in multiple processes occurring later in development, including the location and duration of cell division and cell elongation. The tube growth curves of the small‐floweredM. parishiiand large‐floweredM. lewisiiare essentially indistinguishable, except thatM. parishiitubes stop growing earlier at a smaller size, suggesting a critical role of heterochrony in the shift from outcrossing to selfing. These results not only highlight the developmental process associated with corolla tube variation among species but also provide a baseline reference for future developmental genetic analyses of mutants or transgenic plants with altered corolla tube morphology in this emerging model system.

     
    more » « less
  4. Summary

    Evolution of complex phenotypes depends on the adaptive importance of individual traits, and the developmental changes required to modify traits. Floral syndromes are complex adaptations to pollinators that include color, nectar, and shape variation. Hummingbird‐adapted flowers have evolved a remarkable number of times from bee‐adapted ancestors inPenstemon, and previous work demonstrates that color over shape better distinguishes bee from hummingbird syndromes. Here, we examined the relative importance of nectar volume and nectary development in definingPenstemonpollination syndromes.

    We tested the evolutionary association of nectar volume and nectary area with pollination syndrome across 19Penstemonspecies. In selected species, we assessed cellular‐level processes shaping nectary size. Within a segregating population from an intersyndrome cross, we assessed trait correlations between nectar volume, nectary area, and the size of stamens on which nectaries develop.

    Nectar volume and nectary area displayed an evolutionary association with pollination syndrome. These traits were correlated within a genetic cross, suggesting a mechanistic link. Nectary area evolution involves parallel processes of cell expansion and proliferation.

    Our results demonstrate that changes to nectary patterning are an important contributor to pollination syndrome diversity and provide further evidence that repeated origins of hummingbird adaptation involve parallel developmental processes inPenstemon.

     
    more » « less
  5. Summary

    The mechanisms underlying trait conservation over long evolutionary time scales are poorly known. These mechanisms fall into the two broad and nonmutually exclusive categories of constraint and selection. A variety of factors have been hypothesized to constrain trait evolution. Alternatively, selection can maintain similar trait values across many species if the causes of selection are also relatively conserved, while many sources of constraint may be overcome over longer periods of evolutionary divergence. An example of deep trait conservation is tetradynamy in the large family Brassicaceae, where the four medial stamens are longer than the two lateral stamens. Previous work has found selection to maintain this difference in lengths, which we call anther separation, in wild radish,Raphanus raphanistrum.

    Here, we test the constraint hypothesis using five generations of artificial selection to reduce anther separation in wild radish.

    We found a rapid linear response to this selection, with no evidence for depletion of genetic variation and correlated responses to this selection in only four of 15 other traits, suggesting a lack of strong constraint.

    Taken together, available evidence suggests that tetradynamy is likely to be conserved due to selection, but the function of this trait remains unclear.

     
    more » « less