Population viability of the orchid Gymnadenia conopsea increases with population size but is not related to genetic diversity

Abstract

1 INTRODUCTION

Reductions in population size, often associated with habitat fragmentation, pose challenges for plant populations from both a demographic and genetic point of view. First, demographic and environmental stochasticity is a greater threat for smaller populations. This is because failed reproduction or death of even a few individuals have a large influence on population dynamics, potentially leading to increased risk of extinction (Lande, 1993, 1998). Second, in small populations, individuals have lower chance of mutualistic interactions and fewer mating opportunities, potentially increasing inbreeding (Raijmann et al., 1994), and lowering seed output (Ågren, 1996; Brys et al., 2004). Third, in small populations, the impact of genetic drift is expected to be strong, and fixation of mildly deleterious alleles will cause reductions in individual fitness (Oakley & Winn, 2012; Reed, 2005). Reduced genetic diversity further leads to lower overall adaptive potential and resilience to, for example, diseases and changes in environmental conditions (Hoffmann & Sgrò, 2011). Thus, understanding the consequences of a population's size for both demographic and genetic properties that determine current viability and evolutionary potential is important for conservation priorities.

The expected close relationship between population size and genetic and demographic processes has inspired studies that examine links between population size and genetic diversity (Honnay & Jacquemyn, 2007; Lammi et al., 1999; Leimu et al., 2006), population size and inbreeding depression (Michaels et al., 2008; Oakley & Winn, 2012), and population size and components of fitness (Menges, 1991; Morgan, 1999). However, few studies have directly examined relationships between genetic and demographic properties of plant populations, using metrics that integrate demographic effects across the whole life cycle (e.g. long-term population growth rate, extinction probability). A few existing studies document an association between genetic erosion and reduced population viability (Endels et al., 2007; Hens et al., 2017), whereas others found weak or no effect of genetic diversity on population dynamics (Carley et al., 2022; Fréville et al., 2004; Menges & Dolan, 1998). Such variation in the relationship between genetics and demography could not only reflect differences in ecological context, evolutionary history and mating system (Carley et al., 2022), but also the power to detect an association. Both a high number of populations and years will be necessary to capture a sufficient range in genetic diversity and provide a reliable estimate of population viability of perennial plants. Thus, to clarify the interplay between genetic diversity and population dynamics, further studies that directly link estimates of contemporaneous genetic and demographic metrics at relevant spatial and temporal scales are needed. This is also key to answering which metric will be most useful for predicting future persistence of populations of conservation interest (Carley et al., 2022).

In this study, we combine genome-wide genetic diversity estimates based on 1200 single nucleotide polymorphisms (SNPs), with 6 years of demographic data from 18 populations of the orchid Gymnadenia conopsea (L.) Br. R. on Öland, an island in the Baltic sea in southeastern Sweden. G. conopsea is strongly declining in southern Scandinavia, but still common on Öland, which is a core distribution area in Sweden. Many of the populations harbour high genetic diversity, and genetic differentiation is mostly moderate to low. Still, controlled crosses within and between populations indicate the presence of substantial drift load, particularly in sparse populations (Söderquist et al., 2020). This suggests that also on Öland, some G. conopsea populations are markedly influenced by drift, making this an interesting system to study links between genetic diversity and population dynamics. Here, we use integral projection models (IPM) to relate population dynamics to population size and genetic diversity of the 18 G. conopsea populations. IPMs are especially suited for modelling population dynamics of species that mainly have continuous size variation, but still undergo discrete life stages, for example, dormancy (Jacquemyn et al., 2010b; Merow et al., 2014). We also combine the demographic data with estimates of heterosis from earlier controlled crosses, conducted in 16 of the 18 populations. Specifically, we investigate whether (i) stochastic population growth rate varies among populations, and which demographic rates contribute to this variation, (ii) stochastic population growth rate increases with genetic diversity and population size, (iii) the probability of extinction and strong (90%) decreases in population size within the next 30 years vary among populations and (iv) stochastic population growth rate is lower in populations that expressed strong heterosis in previous crosses.