The Landscape Genetic Signature of Pollination by Trapliners: Evidence From the Tropical Herb, Heliconia tortuosa

Animal-mediated pollination is essential for the maintenance of plant reproduction, especially in tropical ecosystems, where pollination networks have been thought to have highly generalized structures. However, accumulating evidence suggests that not all floral visitors provide equally effective po...

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Main Authors: Felipe Torres-Vanegas, Adam S. Hadley, Urs G. Kormann, Frank Andrew Jones, Matthew G. Betts, Helene H. Wagner
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-12-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fgene.2019.01206/full
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spelling doaj-fc87bcf97a8443358aa0c690a1962af52020-11-25T01:42:35ZengFrontiers Media S.A.Frontiers in Genetics1664-80212019-12-011010.3389/fgene.2019.01206491939The Landscape Genetic Signature of Pollination by Trapliners: Evidence From the Tropical Herb, Heliconia tortuosaFelipe Torres-Vanegas0Adam S. Hadley1Adam S. Hadley2Urs G. Kormann3Frank Andrew Jones4Frank Andrew Jones5Matthew G. Betts6Helene H. Wagner7Department of Ecology and Evolutionary Biology, University of Toronto, Mississauga, ON, CanadaDepartment of Ecology and Evolutionary Biology, University of Toronto, Mississauga, ON, CanadaForest Biodiversity Research Network, Department of Forest Ecosystems and Society, Oregon State University, Corvallis, OR, United StatesSwiss Ornithological Institute, Sempach, SwitzerlandDepartment of Botany and Plant Pathology, Oregon State University, Corvallis, OR, United StatesSmithsonian Tropical Research Institute, Panama, PanamaForest Biodiversity Research Network, Department of Forest Ecosystems and Society, Oregon State University, Corvallis, OR, United StatesDepartment of Ecology and Evolutionary Biology, University of Toronto, Mississauga, ON, CanadaAnimal-mediated pollination is essential for the maintenance of plant reproduction, especially in tropical ecosystems, where pollination networks have been thought to have highly generalized structures. However, accumulating evidence suggests that not all floral visitors provide equally effective pollination services, potentially reducing the number of realized pollinators and increasing the cryptic specialization of pollination networks. Thus, there is a need to understand how different functional groups of pollinators influence pollination success. Here, we examined whether patterns of contemporary pollen-mediated gene flow in Heliconia tortuosa are consistent with the foraging strategy of its territorial or traplining hummingbird pollinators. Territorial hummingbirds defend clumps of flowers and are expected to transfer pollen locally. In contrast, traplining hummingbirds forage across longer distances, thereby increasing pollen flow among forest fragments, and are thought to repeatedly visit particular plants. If trapliners indeed visit the same plants repeatedly along their regular routes, this could lead to a situation where neighboring plants sample genetically distinct pollen pools. To test this hypothesis, we genotyped 720 seeds and 71 mother plants from 18 forest fragments at 11 microsatellite loci. We performed TwoGener analysis to test pollen pool differentiation within sites (among neighboring plants within the same forest fragment: ΦSC) and between sites (among forest fragments: ΦCT). We found strong, statistically significant pollen pool differentiation among neighboring mother plants (ΦSC = 0.0506), and weaker, statistically significant differentiation among sites (ΦCT = 0.0285). We interpret this pattern of hierarchical pollen pool differentiation as the landscape genetic signature of the foraging strategy of traplining hummingbirds, where repeatable, long-distance, and high-fidelity routes transfer pollen among particular plants. Although H. tortuosa is also visited by territorial hummingbirds, our results suggest that these pollinators do not contribute substantially to successful pollination, highlighting differences in realized pollination efficiency. This cryptic reduction in the number of realized pollinators potentially increases the vulnerability of pollination success to the decline of populations of traplining hummingbirds, which have been shown to be sensitive to forest fragmentation. We conclude that maintaining habitat connectivity to sustain the foraging routes of trapliners may be essential for the maintenance of pollen-mediated gene flow in human-modified landscapes.https://www.frontiersin.org/article/10.3389/fgene.2019.01206/fullgene flowhummingbirdpollen pool differentiationpollination networkpollinator recognitionTwoGener
collection DOAJ
language English
format Article
sources DOAJ
author Felipe Torres-Vanegas
Adam S. Hadley
Adam S. Hadley
Urs G. Kormann
Frank Andrew Jones
Frank Andrew Jones
Matthew G. Betts
Helene H. Wagner
spellingShingle Felipe Torres-Vanegas
Adam S. Hadley
Adam S. Hadley
Urs G. Kormann
Frank Andrew Jones
Frank Andrew Jones
Matthew G. Betts
Helene H. Wagner
The Landscape Genetic Signature of Pollination by Trapliners: Evidence From the Tropical Herb, Heliconia tortuosa
Frontiers in Genetics
gene flow
hummingbird
pollen pool differentiation
pollination network
pollinator recognition
TwoGener
author_facet Felipe Torres-Vanegas
Adam S. Hadley
Adam S. Hadley
Urs G. Kormann
Frank Andrew Jones
Frank Andrew Jones
Matthew G. Betts
Helene H. Wagner
author_sort Felipe Torres-Vanegas
title The Landscape Genetic Signature of Pollination by Trapliners: Evidence From the Tropical Herb, Heliconia tortuosa
title_short The Landscape Genetic Signature of Pollination by Trapliners: Evidence From the Tropical Herb, Heliconia tortuosa
title_full The Landscape Genetic Signature of Pollination by Trapliners: Evidence From the Tropical Herb, Heliconia tortuosa
title_fullStr The Landscape Genetic Signature of Pollination by Trapliners: Evidence From the Tropical Herb, Heliconia tortuosa
title_full_unstemmed The Landscape Genetic Signature of Pollination by Trapliners: Evidence From the Tropical Herb, Heliconia tortuosa
title_sort landscape genetic signature of pollination by trapliners: evidence from the tropical herb, heliconia tortuosa
publisher Frontiers Media S.A.
series Frontiers in Genetics
issn 1664-8021
publishDate 2019-12-01
description Animal-mediated pollination is essential for the maintenance of plant reproduction, especially in tropical ecosystems, where pollination networks have been thought to have highly generalized structures. However, accumulating evidence suggests that not all floral visitors provide equally effective pollination services, potentially reducing the number of realized pollinators and increasing the cryptic specialization of pollination networks. Thus, there is a need to understand how different functional groups of pollinators influence pollination success. Here, we examined whether patterns of contemporary pollen-mediated gene flow in Heliconia tortuosa are consistent with the foraging strategy of its territorial or traplining hummingbird pollinators. Territorial hummingbirds defend clumps of flowers and are expected to transfer pollen locally. In contrast, traplining hummingbirds forage across longer distances, thereby increasing pollen flow among forest fragments, and are thought to repeatedly visit particular plants. If trapliners indeed visit the same plants repeatedly along their regular routes, this could lead to a situation where neighboring plants sample genetically distinct pollen pools. To test this hypothesis, we genotyped 720 seeds and 71 mother plants from 18 forest fragments at 11 microsatellite loci. We performed TwoGener analysis to test pollen pool differentiation within sites (among neighboring plants within the same forest fragment: ΦSC) and between sites (among forest fragments: ΦCT). We found strong, statistically significant pollen pool differentiation among neighboring mother plants (ΦSC = 0.0506), and weaker, statistically significant differentiation among sites (ΦCT = 0.0285). We interpret this pattern of hierarchical pollen pool differentiation as the landscape genetic signature of the foraging strategy of traplining hummingbirds, where repeatable, long-distance, and high-fidelity routes transfer pollen among particular plants. Although H. tortuosa is also visited by territorial hummingbirds, our results suggest that these pollinators do not contribute substantially to successful pollination, highlighting differences in realized pollination efficiency. This cryptic reduction in the number of realized pollinators potentially increases the vulnerability of pollination success to the decline of populations of traplining hummingbirds, which have been shown to be sensitive to forest fragmentation. We conclude that maintaining habitat connectivity to sustain the foraging routes of trapliners may be essential for the maintenance of pollen-mediated gene flow in human-modified landscapes.
topic gene flow
hummingbird
pollen pool differentiation
pollination network
pollinator recognition
TwoGener
url https://www.frontiersin.org/article/10.3389/fgene.2019.01206/full
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