Modularity increases rate of floral evolution and adaptive success for functionally specialized pollination systems

Abstract

Angiosperm flowers have diversified in adaptation to pollinators, but are also shaped by developmental and genetic histories. The relative importance of these factors in structuring floral diversity remains unknown. We assess the effects of development, function and evolutionary history by testing competing hypotheses on floral modularity and shape evolution in Merianieae (Melastomataceae). Merianieae are characterized by different pollinator selection regimes and a developmental constraint: tubular anthers adapted to specialized buzz-pollination. Our analyses of tomography-based 3-dimensional flower models show that pollinators selected for functional modules across developmental units and that patterns of floral modularity changed during pollinator shifts. Further, we show that modularity was crucial for Merianieae to overcome the constraint of their tubular anthers through increased rates of evolution in other flower parts. We conclude that modularity may be key to the adaptive success of functionally specialized pollination systems by making flowers flexible (evolvable) for adaptation to changing selection regimes.

Pollination syndromes in the 21stcentury: where do we stand and where may we go?

“…Tansley review New Phytologist Table 1 Methods for data acquisition -compilation of floral traits which may be studied under a pollination biological perspective to expand our understanding of pollination syndromes. Fresh or ethanol-preserved flower material, (herbarium specimens) Advertisement, deterrence, efficiency (Muchhala, 2007;G omez et al, 2016;Smith & Kriebel, 2018; Ben ıtez-Vieyra et al, 2019), traditional syndrome character (Sapir et al, 2017), efficiency (Armbruster et al, 2009;Xiao et al, 2017;Dellinger et al, 2019c) Size (length and width of anthers, filaments etc. )…”

“…Over the past 150 years, the concept of pollination syndromes has been formulated and continuously refined to serve as a large‐scale framework for structuring this diversity in floral mode from a functional, pollination‐ecological perspective (Delpino, 1873–1874; Vogel, 1954; Stebbins, 1970; Faegri & van der Pijl, 1979; Endress, 1996; Ollerton et al ., 2009; Rosas‐Guerrero et al ., 2014). Generally, pollination syndromes represent convergent floral adaptations to specific functional pollinator groups (Smith & Kriebel, 2018; Dellinger et al ., 2019c). Importantly, there is no strict definition on how to delimit syndromes (e.g.…”

Schrödinger's phenotypes: Herbarium specimens show two‐dimensional images are both good and (not so) bad sources of morphological data

“…These differences could bias biological interpretations (Yezerinac et al, 1992) of studies relying on acquisition of morphological data, such as phenotypic evolution, disparity, modularity, phylogenetic inference and others (e.g. Castiglione et al., 2019; Catalano, Goloboff, & Giannini, 2010; Dellinger et al., 2019; Gallaher et al., 2019; Guillerme & Cooper, 2018; Klingenberg & Gidaszewski, 2010; Vasconcelos et al., 2018; Wiens, 2003; Zaragüeta‐Bagils & Bourdon, 2007).…”

Pollen dispensing schedules in buzz-pollinated plants: Experimental comparison of species with contrasting floral morphologies

“…Because anther wall area and anther locule volume are linked, we are potentially detecting the effects of locule volume rather than locule wall area. Quantifying the internal volume of anther locules is difficult but possible using techniques such as X-ray micro-computer tomography scanning (Dellinger et al, 2019a), and our work suggests that this is likely an important variable to measure. The lack of a statistically significant association between pore size and pollen release parameters is intriguing, but perhaps not unexpected given smaller variation in pore sizes than anther areas (see Fig.…”