Assessing Population Genetic Status for Designing Plant Translocations

Abstract

Assisted gene flow interventions such as plant translocations are valuable complementary techniques to habitat restoration. Bringing new genetic variants can contribute to increasing genetic diversity and evolutionary resilience, counteract inbreeding depression and improve plant fitness through heterosis. Large, highly genetically variable populations are usually recommended as sources for translocation. Unfortunately, many critically endangered species only occur as small populations, which are expected to show low genetic variation, high inbreeding level, paucity of compatible mates in self-incompatible species, and increased genetic divergence. Therefore, assessment of population genetic status is required for an appropriate choice of the source populations. In this paper, we exemplify the different analyses relevant for genetic evaluation of populations combining both molecular (plastid and nuclear) markers and fitness-related quantitative traits. We assessed the genetic status of the adult generation and their seed progeny (the potential translocation founders) of small populations of Campanula glomerata (Campanulaceae), a self-incompatible insect-pollinated herbaceous species critically endangered in Belgium. Only a few small populations remain, so that the species has been part of a restoration project of calcareous grasslands implementing plant translocations. In particular, we estimated genetic diversity, inbreeding levels, genetic structure in adults and their seed progeny, recent bottlenecks, clonal extent in adults, contemporary gene flow, effective population size (Ne), and parentage, sibship and seed progeny fitness variation. Small populations of C. glomerata presented high genetic diversity, and extensive contemporary pollen flow within populations, with multiple parentage among seed progenies, and so could be good seed source candidates for translocations. As populations are differentiated from each other, mixing the sources will not only optimize the number of variants and of compatible mates in translocated populations, but also representativeness of species regional genetic diversity. Genetic diversity is no immediate threat to population persistence, but small Ne, restricted among-population gene flow, and evidence of processes leading to genetic erosion, inbreeding and inbreeding depression in the seed progeny require management measures to counteract these trends and stochastic vulnerability. Habitat restoration facilitating recruitment, flowering and pollination, reconnecting populations by biological corridors or stepping stones, and creating new populations through translocations in protected areas are particularly recommended.

Sibship and parentage reconstruction as genetic tool for designing and monitoring plant translocations

“…Contemporary N e estimates in translocated populations are about twice those found in wild populations, but they are small compared to N e estimated from sibship assignment (based on 15 microsatellite loci) for translocated populations of the self‐incompatible Campanula glomerata ( N e ranging from 100 to 178), which also involved large founding population sizes (500 transplants from several small source populations, with N e ranging from 6 to 40), high overall genetic diversity and mixed‐planting design favoring between‐source admixture (Van Rossum et al unpublished data; Van Rossum et al 2022), that is, recommendations to optimize translocation success (e.g. Menges 2008; Hoban et al 2018; Van Rossum et al 2020).…”

“…Menges 2008; Hoban et al 2018; Gargiulo et al 2021). Not only overall genetic diversity in the transplants (the founders of the translocated populations) is important, but also individual genetic quality, that is, the way genetic diversity is partitioned among founders and how founders are genetically related to each other, which depends on outcrossing or selfing levels, and on contemporary pollen dispersal among individuals and populations (Ritchie & Krauss 2012; Frankham et al 2019; Van Rossum et al 2022). For instance, due to pollination failure the founders may result from selfing (in case of self‐compatible species), or be genetically related and belong to a few large families, that is, they consist of full sibs (sharing both parents) and half sibs (sharing one of the two parents).…”

“…Therefore, sibship and parentage reconstruction can give insight into founder or new recruit genetic quality and assess whether contributions to offspring production are spread over a maximum of parents. However, N e , sibship, and/or parentage have been still overlooked for designing and monitoring plant translocations (Krauss et al 2002; Ritchie & Krauss 2012; Gargiulo et al 2021; Thomas et al 2021; Van Rossum et al 2022), despite that thanks to planting protocols, plants can be mapped and the successive generations identified.…”

Genetic diversity assessment of Helichrysum arenarium (Asteraceae) for the genetic restoration of declining populations

“…Assessment of genetic diversity of populations of critically endangered species has been recognized as important for the preparation of restoration projects, and genetic restoration as an essential goal in conservation achievements (e.g., Broadhurst et al., 2023; De Vitis et al., 2022; Mijangos et al., 2015; Wei et al., 2023). Indeed, genetic tools allow for identifying a number of key processes involved in population viability, in particular for plant species: mating processes, genetic erosion, inbreeding, pollen and seed dispersal, sexual recruitment, clonal extent, and progeny genetic quality (Aguilar et al., 2019; Doyle et al., 2023; Van Rossum, 2023; Van Rossum et al., 2022). Depending on the identified failures, additional interventions to ecological restoration may be required to achieve demographically and genetically viable and evolutionary resilient populations (De Vitis et al., 2022; Gargiulo et al., 2021; Ottewell et al., 2016).…”

Translocations of threatened plants in the Mediterranean Basin: current status and future directions

“…Conservation Translocation (translocation hereafter) is an umbrella term that refers to the deliberate movement of living organisms from one area to another for conservation purposes and it consists of either reinforcement plus reintroduction or introduction plans (IUCN/SSC 2013), with the goal of establishing resilient and self-sustaining populations and improving species survival in the wild over time (Menges 2008;; this objective could be pursued through the augmentation of numbers of individuals in small and declining populations, the reintroduction of individuals to extinct populations, or the funding of new safe locations (e.g., Commander et al 2018;Fenu et al 2019). Among the implications related to this concept, plant translocation has also been proposed as a useful action to enhance the genetic parameters of a population, for example, by acting as "bridges" or "connectors" to promote gene flow between isolated populations (e.g., Lázaro-Nogal et al 2017;Bontrager and Angert 2019;Van Rossum et al 2022). Recently, because of the increased interest in the effects of climate change, this term also includes Assisted Migrations or Assisted colonization, aimed to actively support range shifts toward newly suitable areas as an effective climate change adaptation strategy (Thomas 2011;Hällfors et al 2014;Casazza et al 2021;Diallo et al 2021).…”