Novel adaptation to hawkmoth pollinators in Clarkia reduces efficiency, not attraction of diurnal visitors

Miller, Timothy J.; Raguso, Robert A.; Kay, Kathleen M.

doi:10.1093/aob/mct237

Cited by 32 publications

(38 citation statements)

References 82 publications

(103 reference statements)

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“…; Miller et al . ). Fluctuations in hawkmoth abundance may therefore have cascading effects on mating and population dynamics in sphingophilous plants (Raguso & Willis ), and these effects may be further magnified for patchily distributed species in fragmented habitats (Breed et al .…”

Section: Discussionmentioning

confidence: 97%

“…Another critical behavioural distinction lies in grooming, which can bear heavily on pollen transfer dynamics (Wilson & Thomson 1991). Most of the solitary bees observed in our system collect pollen and groom it from their bodies (Gregory 1963(Gregory , 1964, whereas hawkmoths do not (Brunet & Holmquist 2009;Miller et al 2014). Grooming is expected to result in greater pollen removal but lower pollen deposition on a per-visit basis (Castellanos et al 2003) and also cause rapid declines in pollen carryover among flowers relative to nongrooming floral visitors (Thomson 1986;Harder & Wilson 1998;Castellanos et al 2003).…”

Section: Pollinator Identity and Mating Dynamicsmentioning

confidence: 99%

“…Coupled with the fitness consequences of pollinator identity (bee-pollinated flowers are estimated to set 27-33% less seed than hawkmothand open-pollinated flowers, respectively; Skogen et al 2016) declines in hawkmoth abundance could have pronounced impacts on the population dynamics of O. harringtonii. Although hawkmoth visitation to O. harringtonii has been fairly consistent throughout its range over four years of study (Skogen et al 2016), fluctuations in hawkmoth visitation may be a legitimate factor in the long-term population dynamics of other sphingophilous taxa, as hawkmoth abundance has been shown to vary substantially in both space and time (Miller 1981;Campbell et al 1997;Sime & Baldwin 2003;Kulbaba & Worley 2008;Artz et al 2010;Miller et al 2014). Fluctuations in hawkmoth abundance may therefore have cascading effects on mating and population dynamics in sphingophilous plants (Raguso & Willis 2003), and these effects may be further magnified for patchily distributed species in fragmented habitats (Breed et al 2012).…”

Section: Consequences Of Variation In Multiple Paternitymentioning

confidence: 99%

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Pollinator identity and spatial isolation influence multiple paternity in an annual plant

Rhodes

Fant²,

Skogen³

2017

Molecular Ecology

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The occurrence and extent of multiple paternity is an important component of variation in plant mating dynamics. However, links between pollinator activity and multiple paternity are generally lacking, especially for plant species that attract functionally diverse floral visitors. In this study, we separated the influence of two functionally distinct floral visitors (hawkmoths and solitary bees) and characterized their impacts on multiple paternity in a self-incompatible, annual forb, Oenothera harringtonii (Onagraceae). We also situated pollinator-mediated effects in a spatial context by linking variation in multiple paternity to variation in plant spatial isolation. We documented pronounced differences in the number of paternal sires as function of pollinator identity: on average, the primary pollinator (hawkmoths) facilitated mating with nearly twice as many pollen donors relative to the secondary pollinator (solitary bees). This effect was consistent for both isolated and nonisolated individuals, but spatial isolation imposed pronounced reductions on multiple paternity regardless of pollinator identity. Considering that pollinator abundance and pollen dispersal distance did not vary significantly with pollinator identity, we attribute variation in realized mating dynamics primarily to differences in pollinator morphology and behaviour as opposed to pollinator abundance or mating incompatibility arising from underlying spatial genetic structure. Our findings demonstrate that functionally distinct pollinators can have strongly divergent effects on polyandry in plants and further suggest that both pollinator identity and spatial heterogeneity have important roles in plant mating dynamics.

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Section: Discussionmentioning

confidence: 97%

Section: Pollinator Identity and Mating Dynamicsmentioning

confidence: 99%

Section: Consequences Of Variation In Multiple Paternitymentioning

confidence: 99%

See 1 more Smart Citation

Pollinator identity and spatial isolation influence multiple paternity in an annual plant

Rhodes

Fant²,

Skogen³

2017

Molecular Ecology

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“…It has been suggested that these morphological types are associated with pollinators that differ in body size, morphology, and behavior (Willmer, ). Floral morphologies determine pollinator efficiency in that they manipulate the behavior of floral visitors, directly affecting the ways those animals contact flowers and the success of pollen import and export (Wilson, ; Muchhala, ; Ollerton et al., ; Miller et al., ). It is therefore not surprising that switches in morphological types among closely related plants usually accompany switches in pollinators and result in significant trade‐offs in pollination efficiency of different pollinators (Fernández‐Mazuecos, ; Boberg et al., ; Miller et al., ).…”

mentioning

confidence: 99%

Floral adaptations of two lilies: implications for the evolution and pollination ecology of huge trumpet‐shaped flowers

Chang-qiu

Gao

Yang

et al. 2019

American J of Botany

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Premise Evolutionary transitions among floral morphologies, many of which provide evidence for adaptation to novel pollinators, are common. Some trumpet‐shaped flowers are among the largest flowers in angiosperms, occurring in different lineages. Our goal was to investigate the role of pollinators in the evolution of these flowers using Lilium. Methods We investigated floral traits and pollinators of L. primulinum var. ochraceum and L. brownii var. viridulum and reviewed reports of visitors to huge trumpet‐shaped flowers. Using a published phylogeny of Lilium, we reconstructed ancestral floral morphological states in Lilium to elucidate the origins of trumpet‐shaped lilies. Results Both lilies are largely self‐incompatible and show floral syndromes indicative of hawkmoth pollination. The short trumpet‐shaped lily can be pollinated by short‐tongued (<40 mm) but not long‐tongued hawkmoths (>65 mm), while the huge trumpet‐shaped lily can be pollinated by both. A literature review including 22 species of trumpet‐shaped flowers suggests that their pollinator guilds commonly include both short‐ and long‐tongued moths. A phylogenetic reconstruction indicates that trumpet‐shaped lilies possibly have multiple origins from tepal‐reflexed ancestors, at least six of which have evolved huge flowers (>50 mm). Conclusions Adaptation to short‐tongued hawkmoths may have initiated the evolution of trumpet‐shaped lilies. Huge trumpet‐shaped lilies may have evolved as a response to selection by long‐tongued hawkmoths, without excluding the short‐tongued ones. This evolutionary pathway leads to a functionally more generalized pollination system instead of an increasingly specialized one and is not necessarily associated with pollinator shifts.

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“…Types of prezygotic barriers in plants include ecogeographic or habitat isolation (Ramsey et al, 2003;Angert and Schemske, 2005), temporal isolation through flowering time differences (Lowry et al, 2008), pollinator isolation (Hodges et al, 2002;Miller et al, 2014), and postpollination isolation that can occur due to genetic incompatibilities of stigma and style (Kay, 2006). Post-zygotic barriers prevent gene flow after a zygote is formed and include hybrid inviability (Christie and Macnair, 1987) and reduced hybrid fitness (Kay, 2006).…”

Section: Introductionmentioning

confidence: 99%

How are rare species maintained?: Reproductive barriers between Layia jonesii, a rare serpentine endemic, and L. platyglossa

Rossington¹

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Reproductive barriers are vital to generating new species as well as maintaining distinct species. Investigating reproductive barriers between closely related plant taxa helps us to understand how these barriers are maintained, particularly between rare and widespread relatives. Layia jonesii, a rare San Luis Obispo County serpentine endemic, and L. platyglossa, a common coastal species, co-occur on serpentine derived hillsides and are interfertile. At these locations, L. jonesii is isolated to dry soils near serpentine rock outcrops and L. platyglossa is located on slightly deeper grassland soils surrounding the rock outcrops. On hillsides where they co-occur, I observe two morphologically distinct species, therefore the two species must be maintaining reproductive barriers, yet mechanisms that maintain this isolation are unknown. I studied this system to investigate possible mechanisms contributing to the maintenance of reproductive barriers. I hypothesize prezygotic reproductive isolation in this system is due to (1) habitat isolation due to local adaptation to differential edaphic environments on the hillside, (2) flowering time differences, and (3) reduced seed set resulting from hybrid crosses. To investigate the local adaptation of L. jonesii and L. platyglossa, I reciprocally transplanted both species into the center of each species' distribution. I also conducted a competition experiment to determine if L. jonesii is sensitive to resource competition beyond its natural distribution. To investigate flowering time differences, I tracked flowering time of both wild and reciprocally transplanted populations. I also performed controlled crosses to determine if heterospecific, or hybrid crosses, result in lowered seed set than conspecific crosses. The reciprocal transplants showed L. platyglossa is locally adapted to the grassland habitat. Local adaptation likely prevents L. playtyglossa from dispersing into the rock outcrop habitat. Results of the competition experiment revealed L. jonesii is sensitive to competition and this may contribute to its constrained distribution to shallow soils. Local adaptation and competition likely contribute to habitat isolation between the two species. I also documented stark differences in flowering time between the species which contributes to reproductive isolation by reducing pollen flow. Hybrid crosses also resulted in lowered seed set than conspecific crosses. These results suggest prezygotic barriers to reproduction likely maintain the majority of isolation between the two species. These results provide insight into mechanisms that maintain reproductive barriers between closely related taxa existing in similar habitats. The results also contribute to our understanding of how rare plants preserve genetic integrity near common and interfertile relatives.iv ACKNOWLEDGMENTS

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Novel adaptation to hawkmoth pollinators in Clarkia reduces efficiency, not attraction of diurnal visitors

Cited by 32 publications

References 82 publications

Pollinator identity and spatial isolation influence multiple paternity in an annual plant

Pollinator identity and spatial isolation influence multiple paternity in an annual plant

Floral adaptations of two lilies: implications for the evolution and pollination ecology of huge trumpet‐shaped flowers

How are rare species maintained?: Reproductive barriers between Layia jonesii, a rare serpentine endemic, and L. platyglossa

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