Mixing gene pools to prevent inbreeding issues in translocated populations of clonal species

Abstract

Assisted gene flow by plant translocations is increasingly implemented for restoring populations of critically endangered species. The success in restoring genetically healthy populations may depend on translocation design, in particular the choice of the source populations. Highly clonal populations may show low genetic diversity despite large census sizes, and disrupted and geitonogamous pollination may result in selfing and inbreeding issues in the offspring intended for translocation. We carried out a genetic monitoring of translocated populations of the clonal Dianthus deltoides using 14 microsatellite markers and quantified fitness traits over two generations (transplants, F1 seed progeny and newly established individuals). Inbreeding levels were higher in the offspring used as transplants than in the adult generation of the source populations, as a result of high clonality and pollination disruption leading to self‐pollination. The F1 generation in translocated populations showed high genetic diversity maintained across generations, diminished inbreeding levels, low genetic differentiation, pollen flow and genetic mixing between the four sources. New individuals were established from seed germination. Fitness patterns were a combination of inbreeding depression in inbred transplants and F1 progeny, heterosis in admixed F1 progeny, source population adaptive capacities, phenotypic plasticity, maternal effects and site environmental specificities. The strategy in the translocation design to mix several local sources, combined with large founding population sizes and ecological management has proved success in initiating the processes leading to the establishment of genetically healthy populations, even when source populations are highly clonal with low genetic diversity leading to inbreeding issues in the transplants.

Assessing Population Genetic Status for Designing Plant Translocations

“…Populations characterized by high clonal propagation in the adults sampled for translocation material (cuttings, seeds) may show a reduced number of genotypes and of compatible mates compared to what could be expected given census population size, and high inbreeding levels in the seed progeny intended to be used for translocation (Van Rossum and Raspé, 2018;Bittebiere et al, 2020;Van Rossum and Le Pajolec, 2021;.…”

“…Plant translocations consist of intentionally introducing individuals (seeds, cuttings or plug plants) in genetically depauperate, inbred or extirpated populations that cannot recover through pollen flow or through recolonization by seeds from soil seed banks or from nearby populations (Menges, 2008;Weeks et al, 2011). Bringing new genetic variants can contribute to increasing genetic diversity and evolutionary resilience, counteract inbreeding depression and improve plant fitness through heterosis (Zavodna et al, 2015;Van Rossum et al, 2020;Van Rossum and Le Pajolec, 2021). However, translocation-based population restoration may fail for several reasons.…”

“…Poor habitat conditions have been reported as a determinant factor in failure, resulting in high mortality of transplants and low recruit establishment (Godefroid et al, 2011;Schäfer et al, 2020;Volis and Blecher, 2021). Other studies found high inbreeding levels in transplants or in their offspring as a result of a low number of genotypes or reduced pollination service in source populations (Krauss et al, 2002;Monks et al, 2021;Van Rossum and Le Pajolec, 2021). If the introduced gene pool is too genetically differentiated from the natural pool or if the propagated transplants originate from several genetically differentiated sources, founders may be maladapted, and outbreeding depression may be found in the outcrossed progeny as a result of a breakdown of the coadapted genes (Edmands, 2007;Bowles et al, 2015;Barmentlo et al, 2018).…”

“…However, in the current habitat fragmentation context, contemporary gene flow may be restricted due to spatial isolation and pollination disruption (e.g., Ghazoul, 2005;Aguilar et al, 2008). As a result, the seed progeny intended to be used as source for translocation may be genetically depauperate and inbred (Van Geert et al, 2008;Van Rossum, 2008;Thomas et al, 2021;Van Rossum and Le Pajolec, 2021). Small, isolated populations may also become genetically differentiated from each other, as a result of inbreeding and genetic drift (Ottewell et al, 2016;Wiberg et al, 2016), with the risk of outbreeding depression (Edmands, 2007;Barmentlo et al, 2018).…”

“…Effective population size (N e ), which represents a more accurate indicator for population viability than census population size, and bottlenecks that populations may have recently incurred, can also be inferred using molecular markers (Chybicki and Burczyk, 2009;Luikart et al, 2010;Wang, 2016). Fitness quantitative traits inform on negative consequences of habitat fragmentation and population size on reproductive success, on inbreeding or outbreeding depression, and on (mal)adaptation, especially when combined with molecular markers (Zavodna et al, 2015;Barmentlo et al, 2018;Borrell et al, 2019;Van Rossum and Le Pajolec, 2021). Identifying phenotypic plasticity and maternal effects may also give insights into adaptive differences and nonneutral genetic variability accounting for population resilience (Nicotra et al, 2015;Hamilton et al, 2017;Van Rossum et al, 2020).…”