Strong gene flow explains lack of mating system variation in the perennial herb, Vincetoxicum hirundinaria, in a fragmented landscape

Liisa Laukkanen,Aino Kalske,J F Scheepens,Pia Mutikainen,Anne Muola,Roosa Leimu

doi:10.1111/njb.03008

Abstract

Fragmented landscapes may have implications for the genetic structure of populations and for the microevolution of plant species. In particular, landscape fragmentation and/or population isolation might affect the evolution of plant mating systems. Here, we study the consequences of landscape fragmentation on the genetic structure of populations of a perennial herb, Vincetoxicum hirundinaria with a mixed mating system. Our study area, the south‐western Finnish archipelago, was formed after the glacial ice sheet started to retreat 12 000 years ago. Due to the isostatic land uplift following the glacial retreat, suitable habitats have been formed gradually, and as a consequence, populations of V. hirundinaria differ in age, size and their degree of isolation in the area. We hypothesized that a mixed‐mating system has been selected for in these populations due to the advantage of self‐fertilization in newly colonized areas and the advantage of outcrossing in adaptation to heterogeneous environments. To test this hypothesis, we collected seeds of open‐pollinated flowers from 13 V. hirundinaria populations differing in size, age and isolation, and used 15 microsatellite markers to perform progeny‐array analysis to estimate population‐level outcrossing rates, population genetic indices and population structure. We found that V. hirundinaria is almost completely outcrossing in the study area with no signs of past self‐fertilization and/or mating among relatives. The overall low inbreeding coefficients indicate that even in small populations mating among relatives is rare. High allelic richness of both maternal and offspring genotypes as well as limited genetic differentiation among the studied populations indicate strong gene flow among them. Our findings suggest that V. hirundinaria has successful seed and pollen dispersal among populations that has allowed colonization of new habitats in this fragmented landscape and led to a genetically well‐mixed group of populations at the scale of the study.

Highlights

Fragmented landscapes, whether natural or man-made, may have implications for the population genetic structure and adaptive evolution of plant species (Hoebee et al 2007)
Our findings suggest that V. hirundinaria has successful seed and pollen dispersal among populations that has allowed colonization of new habitats in this fragmented landscape and led to a genetically well-mixed group of populations at the scale of the study
We found that Vincetoxicum hirundinaria is almost completely outcrossing in the SW archipelago of Finland, which is contrary to our expectation of an increasing amount of selfing in smaller, younger and more isolated populations

Summary

Introduction

Fragmented landscapes, whether natural or man-made, may have implications for the population genetic structure and adaptive evolution of plant species (Hoebee et al 2007). Gene flow should diminish and among population genetic differentiation should increase with increasing population isolation (Young et al 1996, Gómez-Fernández et al 2016). Such developments can, on the one hand, be devastating for the adaptive potential of a species or populations existing in such an environment (Fischer and Matthies 1998, Garant et al 2007). The degree of landscape fragmentation, or the isolation of populations, can have consequences for the evolution of plant mating systems (Llorens et al 2012, Coates et al 2013, Gauli et al 2014, Sampson et al 2014, Breed et al 2015). While selffertilization has been suggested to promote species invasion and establishment into novel or remote habitats (Baker 1955, Pannell 2015) it might be advantageous in fragmented landscapes

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