Pollinator movement activity influences genetic diversity and differentiation of spatially isolated populations of clonal forest herbs

Abstract

In agricultural landscapes, forest herbs live in small, spatially isolated forest patches. For their long-term survival, their populations depend on animals as genetic linkers that provide pollen- or seed-mediated gene flow among different forest patches. However, whether insect pollinators serve as genetic linkers among spatially isolated forest herb populations in agricultural landscapes remains to be shown. Here, we used population genetic methods to analyze: (A) the genetic diversity and genetic differentiation of populations of two common, slow-colonizing temperate forest herb species [Polygonatum multiflorum (L.) All. and Anemone nemorosa L.] in spatially isolated populations within three agricultural landscapes in Germany and Sweden and (B) the movement activity of their most relevant associated pollinator species, i.e., the bumblebee Bombus pascuorum (Scopoli, 1,763) and the hoverfly Melanostoma scalare (Fabricus, 1,794), respectively, which differ in their mobility. We tested whether the indicated pollinator movement activity affected the genetic diversity and genetic differentiation of the forest herb populations. Bumblebee movement indicators that solely indicated movement activity between the forest patches affected both genetic diversity and genetic differentiation of the associated forest herb P. multiflorum in a way that can be explained by pollen-mediated gene flow among the forest herb populations. In contrast, movement indicators reflecting the total movement activity at a forest patch (including within-forest patch movement activity) showed unexpected effects for both plant-pollinator pairs that might be explained by accelerated genetic drift due to enhanced sexual reproduction. Our integrated approach revealed that bumblebees serve as genetic linkers of associated forest herb populations, even if they are more than 2 km apart from each other. No such evidence was found for the forest associated hoverfly species which showed significant genetic differentiation among forest patches itself. Our approach also indicated that a higher within-forest patch movement activity of both pollinator species might enhance sexual recruitment and thus diminishes the temporal buffer that clonal growth provides against habitat fragmentation effects.

Limited effects of population age on the genetic structure of spatially isolated forest herb populations in temperate Europe

“…Different from A. nemorosa, which is associated with shortdistance, forest-specialized pollinators (Feigs et al, 2022), P. multiflorum is pollinated by bumblebees (Kosiński, 2012) that are able to fly over a heterogeneous landscape (Persson & Smith, 2011).…”

“…Young populations of plant species mainly pollinated by far‐reaching vectors, for example, wind, can better overcome the founder effect (Hampe et al., 2013 ). Similarly, for many insect‐pollinated forest herb species in temperate Europe, their pollinators' foraging range and commuting behaviour should affect the distance and frequency of pollen transport among plant populations (Berge et al., 1998 ; Feigs et al., 2022 ; Naaf et al., 2021 ) and thus the strength of the age effect on the population genetic structure.…”

Pollen as the link between floral phenotype and fitness

“…Another important source of variation in pollen‐transfer efficiency is the identity of pollinators. These differences are clear from a small but growing body of studies assessing landscape‐scale effects of pollinator mobility on population differentiation (Dellinger et al, 2022; Feigs et al, 2022; Gamba and Muchhala, 2023). In this issue, Lewis et al (2023) used population genetics to test whether differences in the mobility of hawkmoth and bee pollinators explain population differentiation in two species of Oenothera .…”

Dominance of non-wetland-dependent pollinators in a plant community in a small natural wetland in Shimane, Japan

“…Insects play a vital role in pollinating many wetland plants with sexual reproduction (Kato 1998 ; Kato and Miura 1996 ). While asexual reproduction such as vegetative reproduction can efficiently increase clonal individuals (Da Silva et al 2017 ; Holsinger 2000 ), sexual reproduction is very important for maintaining their genetic diversity (Feigs et al 2022 ; Jeltsch et al 2013 ). Genetic diversity plays an important role in the survival of species because it gives species the ability to adapt in a changing environment (Ouborg et al 2006 ).…”