High levels of effective long-distance dispersal may blur ecotypic divergence in a rare terrestrial orchid

Abstract

BackgroundGene flow and adaptive divergence are key aspects of metapopulation dynamics and ecological speciation. Long-distance dispersal is hard to detect and few studies estimate dispersal in combination with adaptive divergence. The aim of this study was to investigate effective long-distance dispersal and adaptive divergence in the fen orchid (Liparis loeselii (L.) Rich.). We used amplified fragment length polymorphism (AFLP)-based assignment tests to quantify effective long-distance dispersal at two different regions in Northwest Europe. In addition, genomic divergence between fen orchid populations occupying two distinguishable habitats, wet dune slacks and alkaline fens, was investigated by a genome scan approach at different spatial scales (continental, landscape and regional) and based on 451 AFLP loci.ResultsWe expected that different habitats would contribute to strong divergence and restricted gene flow resulting in isolation-by-adaptation. Instead, we found remarkably high levels of effective long-distance seed dispersal and low levels of adaptive divergence. At least 15% of the assigned individuals likely originated from among-population dispersal events with dispersal distances up to 220 km. Six (1.3%) ‘outlier’ loci, potentially reflecting local adaptation to habitat-type, were identified with high statistical support. Of these, only one (0.22%) was a replicated outlier in multiple independent dune-fen population comparisons and thus possibly reflecting truly parallel divergence. Signals of adaptation in response to habitat type were most evident at the scale of individual populations.ConclusionsThe findings of this study suggest that the homogenizing effect of effective long-distance seed dispersal may overwhelm divergent selection associated to habitat type in fen orchids in Northwest Europe.

Window of opportunity of Liparis loeselii populations during vegetation succession on the Wadden Sea islands

“…Several population genetic studies (Pillon et al 2007, Shahrudin 2014, Vanden Broeck et al 2014 provide support for the good seed dispersal although the genetic structure is affected strongly by the spontaneous self-pollination of the species. Assignment tests of juvenile individuals to their most likely population of origin suggest that even though most dispersal occurs over relatively short distances, much longer distances of >100 km are bridged occasionally (Shahrudin 2014, Vanden Broeck et al 2014. Hence, vacant habitat patches are probably colonized quite rapidly in most cases, although we have also observed on Terschelling that a dune slack was suitable for at least 10 years before it was successfully colonized by the species.…”

Seed dispersal in six species of terrestrial orchids in Biebrza National Park (NE Poland)

“…In many or even most of the papers concerning the genetic structure of orchids, high gene flow via seeds is one of the most common explanations for low population differentiation [28,33]. Such an interpretation of genetic data is mainly theoretical because there are no detailed investigations of the effect of long-distance dispersal on genetic diversity in orchids [1,44], excluding some examples [10]. Recently, a few authors have reported that gene flow in orchids via seeds appears to be restricted [16,27,41,[45][46][47][48]].…”

“…Firstly, studies on seed dispersal provide information about important aspects of species biology, which is indispensable to explain different ecological and evolutionary processes. Secondly, data about distances at which seeds are transported, along with knowledge of the distribution of individuals within one population and across populations of a given species within its geographical range, inform us of gene flow between different biological and ecological units [7][8][9][10]. At a time of fragmentation of natural environments and increasing biodiversity threats, knowledge of gene flow via seeds is crucial to determine the connectivity between populations of endangered DOI: 10.5586/asbp.3557…”

“…Data from field observations testing seed dispersal is very scarce, and mostly focused on seeds dispersed by animals, mainly in fleshy-fruited plants [21][22][23][24][25]. Genetic methods, based both on parentage analysis, fine-scale spatial genetic analysis and assignment tests, have also been used to assess the relative contributions of seed dispersal to gene flow [1,10,12,13,[26][27][28][29][30]. We should remember that many genetic studies based on F st (the standardized measure of the genetic variance among populations), although very valuable in explaining gene exchange, do not reflect actual seed dispersal.…”

“…Long-distance dispersal contributes to the emergence of new populations, thus influencing the geographical range of a particular species [3,4]. Moreover, long-distance dispersal events are also important in determining the selection of dispersal structures or adaptation to different environments [7,10,35].…”