Pollinator-mediated selection and floral evolution: from pollination ecology to macroevolution

Special Feature Articles: Commentary

Trait correlates and functional significance of heteranthery in flowering plants

Pollinator-mediated selection and floral evolution: from pollination ecology to macroevolution

Mario Vallejo-Marín, Elizabeth M. Da Silva, Risa D. Sargent and Spencer C. H. Barrett

Yuval Sapir and W. Scott Armbruster

Research reviews Using phylogenetics to detect pollinator-mediated floral evolution Stacey DeWitt Smith

Full papers Direct selection at the blossom level on floral reward by pollinators in a natural population of Dalechampia schottii: full-disclosure honesty?

Pollinator behaviour and plant speciation: can assortative mating and disruptive selection maintain distinct floral morphs in sympatry?

Paul D. Rymer, Steven D. Johnson and Vincent Savolainen

Pollinator specificity, floral odour chemistry and the phylogeny of Australian sexually deceptive Chiloglottis orchids: implications for pollinator-driven speciation Rod Peakall, Daniel Ebert, Jacqueline Poldy, Russell A. Barrow, Wittko Francke, Colin C. Bower and Florian P. Schiestl

Geir H. Bolstad, W. Scott Armbruster, Christophe Pélabon, Rocío Pérez-Barrales and Thomas F. Hansen

Pollinator-mediated selection on floral display, spur length and flowering phenology in the deceptive orchid Dactylorhiza lapponica Nina Sletvold, John M. Grindeland and Jon Ågren

Pollinators exert natural selection on flower size and floral display in Penstemon digitalis Amy L. Parachnowitsch and André Kessler

Evolutionary breakdown of pollination specialization in a Caribbean plant radiation Silvana Martén-Rodríguez, Charles B. Fenster, Ingi Agnarsson, Laurence E. Skog and Elizabeth A. Zimmer

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Introduction Plant–pollinator relationships have been a central topic in the study of floral evolution ever since Darwin (1859, 1862); they have been cited as a classic example of evolution in response to selection mediated through biotic interactions (Grant, 1949; van der Pijl, 1961; FÌgri & van der Pijl, 1979; Proctor et al., 1996).

Many studies have attempted to place pollination ecology in an explicitly evolutionary framework (e.g. Grant, 1949; van der Pijl, 1961; Levin & Kerster, 1967; Schemske & Bradshaw, 1999; Armbruster et al., 2005; Muchhala, 2007; Vereecken et al., 2010).

Nevertheless, there are very few studies in which the full path, from molecular patterns at the genome level and pollinator-mediated selection on phenotype, to the final evolutionary consequences, has been elucidated (Campbell et al., 1991; Bradshaw & Schemske, 2003; Hoballah et al., 2007). It is an ideal time to assess recent progress in taking evolutionary approaches to investigate pollination biology, with the aim of developing a cohesive framework for understanding the role of pollination in floral evolution. This issue of New Phytologist contains a special feature, based partly on a European Society for Evolutionary Biology symposium held in Turin in August 2009, that gathers together studies aimed at advancing our evolutionary understanding of pollination and setting a framework for future work.

Research review Using phylogenetics to detect pollinatormediated floral evolution

Author for correspondence: Stacey DeWitt Smith Tel: +1 919 684 3378 Email: stacey.smith@duke.edu

Stacey DeWitt Smith

Summary New Phytologist (2010) 188: 354–363 doi: 10.1111/j.1469-8137.2010.03292.x

Keywords: ancestral state reconstruction, diversification, floral evolution, phylogenetic generalized least squares, phylogenetics, pollination system, stochastic mapping, transition rate.

The development of comparative phylogenetic methods has provided a powerful toolkit for addressing adaptive hypotheses, and researchers have begun to apply these methods to test the role of pollinators in floral evolution and diversification. One approach is to reconstruct the history of both floral traits and pollination systems to determine if floral trait change is spurred by shifts in pollinators. Looking across multiple shifts, it is also possible to test for significant correlations between floral evolution and pollinators using parsimony, likelihood and Bayesian methods for discrete characters or using statistical comparative methods for continuous characters.

Evolutionary shifts in pollinators and floral traits may cause changes in diversification rates, and new methods are available for simultaneously studying character evolution and diversification rates. Relatively few studies have yet used formal comparative methods to elucidate how pollinators affect floral evolution across the phylogeny, and fruitful directions for future applications are discussed.

Direct selection at the blossom level on floral reward by pollinators in a natural population of Dalechampia schottii: full-disclosure honesty?

Geir H. Bolstad, W. Scott Armbruster, Christophe Pélabon, Rocío Pérez-Barrales and Thomas F. Hansen

Summary Author for correspondence: Geir H. Bolstad Tel: +47 92 03 76 65 Email: geir.bolstad@bio.ntnu.no

New Phytologist (2010) 188: 370–384 doi: 10.1111/j.1469-8137.2010.03429.x

KEYWORDS: Dalechampia schottii, fitness function, euglossine bees, multivariate selection, natural selection, pollination, selection gradient.

Both floral rewards and advertisements can be important in the attraction of pollinators, but few studies have separated the individual contributions of rewards and advertisements to fitness.

Here, we investigated selection by pollinators on individual blossoms in Dalechampia schottii. This Neotropical vine, endemic to the Yucatán Peninsula, rewards bees by secreting fully visible, deep-blue resin from a gland subtended by two conspicuous petaloid bracts that may play the role of advertisement.

We used contextual analysis to build a fitness function for four morphological traits of individual blossoms: the amount of the reward as measured by gland area; the size of the advertisement trait as measured by bract length; the flower-pollinator fit as measured by the shortest distance between reward and stigma; and the potential for self-pollination as measured by the shortest distance between anthers and stigma.

Larger gland area and increased potential for self-pollination directly increased the seed production of individual blossoms. However, bract size or flower-pollinator fit did not influence the number of seeds produced by blossoms. Therefore, in this Dalechampia species, pollinators seem to select directly on the reward of individual blossoms but not on the advertising bracts.

Pollinator-mediated selection on floral display, spur length and flowering phenology in the deceptive orchid Dactylorhiza lapponica Nina Sletvold, John M. Grindeland and Jon Ågren

Summary Author for correspondence: Nina Sletvold Tel: +47 73 592262 Email: nina.sletvold@vm.ntnu.no

Nonrewarding animal-pollinated plants commonly experience severe pollen limitation, which should result in strong selection on traits affecting the success of pollination. However, the importance of pollinators as selective agents on floral traits in deceptive species has not been quantified experimentally.

New Phytologist (2010) 188: 385–392 doi: 10.1111/j.1469-8137.2010.03296.x

Here, we quantified pollinator-mediated selection (Δβpoll) on floral morphology and start of flowering in the deceptive orchid Dactylorhiza lapponica by subtracting estimates of selection gradients for plants receiving supplemental hand-pollination from estimates obtained for open-pollinated control plants.

KEYWORDS: deceptive orchids, female fitness, floral evolution, natural selection,plant–animal interactions, pollen limitation, pollinator-mediated selection, selection

There was directional selection for taller plants with more flowers and longer spurs, but no statistically significant selection on corolla size or flowering start. Pollinatormediated selection accounted for all observed selection on spur length (Δβpoll = 0.32), 76% of the selection on plant height (Δβpoll = 0.19) and 42% of the selection on number of flowers (Δβpoll = 0.30). Sixteen per cent of developing fruits were consumed by insect herbivores, but fruit herbivory had only minor effects on the strength of pollinator-mediated selection.

Our results demonstrate that pollinators mediate selection on floral traits likely to affect both pollinator attraction and pollination efficiency, and are consistent with the hypothesis that deceptive species experience strong selection for increased display and mechanical fit between flower and pollinator.

Pollinators exert natural selection on flower size and floral display in Penstemon digitalis Amy L. Parachnowitsch and AndrĂŠ Kessler

Summary Author for correspondence: Amy L. Parachnowitsch Tel: +1 607 339 3153 Email: alp43@cornell.edu

New Phytologist (2010) 188: 393–402 doi: 10.1111/j.1469-8137.2010.03410.x

KEYWORDS: floral display, flower size, natural selection, Penstemon digitalis, pollinators.

A major gap in our understanding of floral evolution, especially micro-evolutionary processes, is the role of pollinators in generating patterns of natural selection on floral traits. Here we explicitly tested the role of pollinators in selecting floral traits in a herbaceous perennial, Penstemon digitalis.

We manipulated the effect of pollinators on fitness through hand pollinations and compared phenotypic selection in open- and hand-pollinated plants.

Despite the lack of pollen limitation in our population, pollinators mediated selection on floral size and floral display. Hand pollinations removed directional selection for larger flowers and stabilizing selection on flower number, suggesting that pollinators were the agents of selection on both of these traits.

We reviewed studies that measured natural selection on floral traits by biotic agents and generally found stronger signatures of selection imposed by pollinators than by herbivores and co-flowering plant species.

Evolutionary breakdown of pollination specialization in a Caribbean plant radiation Silvana Martén-Rodríguez, Charles B. Fenster, Ingi Agnarsson, Laurence E. Skog and Elizabeth A. Zimmer

Summary Author for correspondence: Silvana Marte´n-Rodrı´guez Tel: +506 2511-5960 Email: smartenr@gmail.com

New Phytologist (2010) 188: 403–417 doi: 10.1111/j.1469-8137.2010.03330.x

KEYWORDS: Antilles, autogamy, floral traits, G-CYCLOIDEA (GCYC), Gesneriaceae, internal transcribed spacer (ITS), islands, phylogeny, pollination systems.

Ecological generalization is postulated to be the rule in plant–pollinator interactions; however, the evolution of generalized flowers from specialized ancestors has rarely been demonstrated. This study examines the evolution of pollination and breeding systems in the tribe Gesnerieae (Gesneriaceae), an Antillean plant radiation that includes specialized and generalized species.

Phylogenetic reconstruction was based on two nDNA markers (internal transcribed spacer (ITS) and G-CYCLOIDEA (GCYC) and morphology. The total evidence Bayesian phylogeny was used for assessment of floral character evolution using Bayesian stochastic character mapping.

Mapping of the pollination system resulted in at least two origins of bat pollination and two origins of generalized pollination (bats, moths and hummingbirds). The evolution of bat pollination was associated with floral transitions reflecting the chiropterophilous floral syndrome. The evolution of generalization was associated with subcampanulate corollas. Autonomous breeding systems evolved only in hummingbird-pollinated lineages.

The correlated evolution of floral traits and pollination systems provides support for the pollination syndrome concept. Floral transitions may have been favored by the low frequency of hummingbird visitation in the Antilles, while the presence of autonomous pollination may have allowed the diversification of ornithophilous lineages. Results suggest that pollinator depauperate faunas on islands select for the evolution of reproductive assurance mechanisms, including generalization and autogamy.

Trait correlates and functional significance of heteranthery in flowering plants Mario Vallejo-Marín, Elizabeth M. Da Silva, Risa D. Sargent and Spencer C. H. Barrett

Summary Author for correspondence: Mario Vallejo-Marı´n Tel: +44 1786 467822 Email: mario.vallejo@stir.ac.uk

Flowering plants display extraordinary diversity in the morphology of male sexual organs, yet the functional significance of this variation is not well understood. Here, we conducted a comparative analysis of floral correlates of heteranthery – the morphological and functional differentiation of anthers within flowers – among angiosperm families to identify traits associated with this condition.

New Phytologist (2010) 187: 941–956 doi: 10.1111/j.1469-8137.2010.03337.x

We performed a phylogenetic analysis of correlated evolution between heteranthery and several floral traits commonly reported from heterantherous taxa. In addition, we quantified the effect of phylogenetic uncertainty in the observed patterns of correlated evolution by comparing trees in which polytomous branches were randomly resolved.

KEYWORDS: buzz-pollination, division of labour, heteranthery, phylogenetic analysis, stamen differentiation.

Heteranthery is reported from 12 angiosperm orders and is phylogenetically associated with the absence of floral nectaries, buzz-pollination and enantiostyly (mirror-image flowers). These associations are robust to particularities of the underlying phylogenetic hypothesis.

Heteranthery has probably evolved as a result of pollinator-mediated selection and appears to function to reduce the conflict of relying on pollen both as food to attract pollinators and as the agent of male gamete transfer. The relative scarcity of heteranthery among angiosperm families suggests that the conditions permitting its evolution are not easily met despite the abundance of pollen-collecting bees and nectarless flowers.

Pollinator behaviour and plant speciation: can assortative mating and disruptive selection maintain distinct floral morphs in sympatry?

Paul D. Rymer, Steven D. Johnson and Vincent Savolainen

Summary Author for correspondence: Paul D. Rymer Tel: +61 415 963 139 Email: paul.rymer@yahoo.com

New Phytologist (2010) 188: 426–436 doi: 10.1111/j.1469-8137.2010.03438.x

KEYWORDS: ecological speciation, gene flow, Gladiolus: Iridaceae, introgression, mating patterns, microsatellite, phenotypic selection, southern Africa.

Pollinators, as gene flow vectors and selection agents, play a central role in the origin and maintenance of floral variation in natural populations. However, it is debatable whether pollination alone can complete the speciation process in sympatry.

Mating patterns and phenotypic selection on floral traits were characterized over two flowering seasons for sympatric corolla tube length morphs of the hawkmoth-pollinated iris Gladiolus longicollis. A mating model with genetic and spatial–temporal predictors was developed to identify seed paternity. A multivariate analysis was used to estimate selection on correlated floral traits based on maternal and paternal fitness.

Mating patterns among floral morphs were density dependent, resulting in assortative mating at low plant densities, and random mating among morphs at high densities. Weak disruptive selection on tube length was detected in one season for maternal fitness. Plant height was under opposing directional selection for maternal (+) and paternal (−) fitness functions.

These results indicate that G. longicollis morphs will introgress rather than diverge towards speciation. The lack of strong assortative mating, particularly at high densities, is predicted to result in the loss of rare morphs within populations, and indicates that spatial and temporal co-occurrences of floral morphs are evolutionarily unstable.

Pollinator specificity, floral odour chemistry and the phylogeny of Australian sexually deceptive Chiloglottis orchids: implications for pollinator-driven speciation Rod Peakall, Daniel Ebert, Jacqueline Poldy, Russell A. Barrow, Wittko Francke, Colin C. Bower and Florian P. Schiestl

Summary Author for correspondence: Rod Peakall Tel: 612 61250022 Email: rod.peakall@anu.edu.au

Sexually deceptive orchids are predicted to represent a special case of plant speciation where strong reproductive isolation may be achieved by differences in floral scent.

New Phytologist (2010) 188: 437–450 doi: 10.1111/j.1469-8137.2010.03308.x

In this study of Australian sexually deceptive Chiloglottis orchids, we performed choice experiments to test for wasp pollinator specificity in the field; identified the compounds involved in pollinator attraction by gas chromatography with electroantennographic detection (GC-EAD), gas chromatography with mass selective detection (GC-MS), chemical synthesis and behavioural bioassays; and mapped our chemical findings on to a phylogeny of the orchids.

KEYWORDS: chemical mimicry, Chiloglottis, diversification, Orchidaceae, pollination, semiochemicals, sexual deception, speciation.

Field experiments confirmed pollination is a highly specific interaction, but also revealed a pool of nonpollinating ‘minor responder’ wasps. Six novel compounds, all 2,5-dialkylcyclohexan-1,3-diones, called ‘chiloglottones’, were discovered to be involved in pollinator attraction. Bioassays confirmed that pollinator specificity has a strong chemical basis, with specificity among sympatric orchids maintained by either different single compounds or a variation in a blend of two compounds. The phylogenetic overlay confirmed that speciation is always associated with pollinator switching and usually underpinned by chemical change.

If the chemical differences that control reproductive isolation in Chiloglottis have a strong genetic basis, and given the confirmed pool of potential pollinators, we conclude that pollinator-driven speciation appears highly plausible in this system.

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