Hawkmoth Pollination Facilitates Long-distance Pollen Dispersal and Reduces Isolation Across a Gradient of Land-use Change

Abstract

Land-use change is among the top drivers of global biodiversity loss, which impacts the arrangement and distribution of suitable habitat for species. Population-level effects include increased isolation, decreased population size, and changes to mutualistic and antagonistic interactions. However, the extent to which species are impacted is determined by life history characteristics including dispersal. In plants, mating dynamics can be changed in ways that can negatively impact population persistence if dispersal of pollen and/or seed is disrupted. Long-distance dispersal has the potential to buffer species from the negative impacts of land-use change. Biotic vectors of long-distance dispersal have been less frequently studied, though specific taxa are known to travel great distances. Here, we describe population genetic diversity and structure in a sphingophilous species that is experiencing habitat fragmentation through land-use change, Oenothera harringtonii W. L. Wagner, Stockh. & W. M. Klein (Onagraceae). We use 12 nuclear and four plastid microsatellite markers and show that pollen dispersal by hawkmoths drives high gene flow and low population differentiation despite a range-wide gradient of land-use change and habitat fragmentation. By separating the contributions of pollen and seed dispersal to gene flow, we show that most of the genetic parameters are driven by hawkmoth-facilitated long-distance pollen dispersal, but populations with small, effective population sizes experience higher levels of relatedness and inbreeding. We discuss considerations for conservation efforts for this and other species that are pollinated by long-distance dispersers.

Global patterns of population genetic differentiation in seed plants

“…Our results did not support the hypothesis that gravity-mediated seed dispersal increases population differentiation compared to wind or animal dispersal (Givnish, 2010) (Figure 2d). This is in line with previous findings suggesting that the genetic structure of nuclear markers is largely driven by pollen flow (Petit et al, 2005;Skogen et al, 2019;Sork, Nason, Campbell, & Fernandez, 1999) and that the effect of seed dispersal is only detectable in the population genetic structure of chloroplast genes (Duminil et al, 2007).…”

“…This pattern is likely due to reduced gene flow among plant populations. In fact, small insects have a lower pollen carry‐over capacity than bumblebees and vertebrates (Dick et al., 2008; Rhodes, Fant, & Skogen, 2017), and studies of pollinator movement show that euglossine bees, hawkmoths and bats can all travel long distances, even across fragmented habitats (Brunet, Larson‐Rabin, & Stewart, 2012; Finger, Kaiser‐Bunbury, Kettle, Valentin, & Ghazoul, 2014; Janzen, 1971; López‐Uribe, Oi, & Del Lama, 2008; McCulloch et al., 2013; Skogen, Overson, Hilpman, & Fant, 2019). Our results show that wind, large insects and vertebrates have similar and statistically indistinguishable homogenizing effects on plant F ST .…”

“…Thus, in order to preserve the largest amount of genetic diversity for species with such traits, conservation efforts should seek to maintain numerous subpopulations spanning a wide geographic extent. Future broad‐scale studies of F ST variation could provide even greater insights for conservation by including population densities (Murawski & Hamrick, 1991; Sork et al., 1999), effects of habitat fragmentation (Aguilar, Quesada, Ashworth, Herrerias‐Diego, & Lobo, 2008; Skogen et al., 2019), and the landscape context of populations (Sork et al., 1999).…”

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

“…Larger bees and moths take longer foraging trips than smaller insects (e.g. Greenleaf et al, 2007;Dick et al, 2008;Skogen et al, 2019), with observed exceptions (e.g. Castilla et al, 2017;O'Connell et al, 2018).…”

Target enrichment and extensive population sampling help untangle the recent, rapid radiation of Oenothera sect. Calylophus

“…Hawkmoth pollination, which is ancestral in the family Onagraceae, and common in Oenothera sect. Calylophus, is known to result in long-distance pollen movement (Stockhouse 1973;Skogen et al 2019); therefore, gene flow may have been extensive over the evolutionary history of hawkmoth-pollinated taxa, increasing the chances that processes such as historical introgression may obscure phylogenetic signal in extant plants (Elrich and Raven 1969). With a phylogenomic approach that samples hundreds of nuclear loci, we may better illuminate both the history of these species and the key evolutionary processes related to speciation in this group.…”