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

Abstract

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: Φ SC) and between sites (among forest fragments: Φ CT). We found strong, statistically significant pollen pool differentiation among neighboring mother plants (Φ SC = 0.0506), and weaker, statistically significant differentiation among sites (Φ CT = 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.

Tropical deforestation reduces plant mating quality by shifting the functional composition of pollinator communities

“…This ‘high‐mobility’ foraging strategy can potentially increase outcrossing and mate diversity by facilitating the receipt of non‐self and unrelated pollen (Ohashi & Thomson, 2009). Our recent work showed that hierarchical patterns of pollen pool differentiation (quantified among forest patches and among neighbouring H. tortuosa individuals within forest patches) were consistent with the foraging strategy of high‐mobility traplining hummingbirds, as neighbouring H. tortuosa individuals were found to sample genetically distinct pollen pools (Torres‐Vanegas et al., 2019). This suggests that these species are largely responsible for effective pollen transfer in H. tortuosa (Torres‐Vanegas et al., 2019).…”

“…Our recent work showed that hierarchical patterns of pollen pool differentiation (quantified among forest patches and among neighbouring H. tortuosa individuals within forest patches) were consistent with the foraging strategy of high‐mobility traplining hummingbirds, as neighbouring H. tortuosa individuals were found to sample genetically distinct pollen pools (Torres‐Vanegas et al., 2019). This suggests that these species are largely responsible for effective pollen transfer in H. tortuosa (Torres‐Vanegas et al., 2019). As such, the next important step is to understand how deforestation and reduced abundance of high‐mobility traplining hummingbirds impact plant mating quality.…”

“…All DNA extractions were completed using the QIAGEN DNeasy Plant Mini Kit following the manufacturer's protocol (QIAGEN). All samples were amplified and genotyped at 11 microsatellite loci (Hac_C7, Hb_C115, Hac_D1, Hb_B9, Hac_B4, Hac_B6, Hac_C114, Hac_A103, Hc_C7, Hac_A116, Hc_C126) and markers were tested for departures from Hardy–Weinberg equilibrium, linkage disequilibrium and null alleles (for details see Torres‐Vanegas et al., 2019). Genotyping errors were scored as the per locus rate of genotype mismatches observed in the maternal plant‐offspring arrays.…”

From pollen dispersal to plant diversification: genetic consequences of pollination mode

“…The flowers of H. tortuosa can recognize and favor pollination by traplining hummingbirds over territorial hummingbirds, as only trapliners fully drain the available nectar – the signal that triggers pollen tube growth (Betts et al ., 2015). This pollinator recognition mechanism results in high realized pollen dispersal, as is expected for pollination by trapliners (Torres‐Vanegas et al ., 2019). The prevalence of such recognition systems is unknown.…”

Global vision of heliconias research as cut flower: a review

“…This species harbors a diversity of organisms beneficial to the environment (Benítez-Malvido et al, 2019;Janeček et al, 2019), and provide an ideal habitat for the development of the biological cycle of some insects corresponding to the orders: Diptera, Coleoptera, Himenoptera y Hemiptera, due to the different phenological, structural and environmental conditions generated in the crops (Henao and Ospina, 2008;Foottit and Maw, 2019). Furthermore, these species are mainly pollinated by hummingbirds and bats (Temeles and Bishop, 2019;Torres-Vanegas et al, 2019). The latter are used by heliconia plants for reproduction and survival; rolled tubular sheets provide microclimatic conditions suitable for tropical species and benefit camouflage (Pérez-Cárdenas et al, 2019; Rodríguez-Herrera et al, 2019).…”