Date Published: April 11, 2019
Publisher: Public Library of Science
Author(s): Demet Çekin, Peter Schausberger, Chung-Ping Lin.
Both close inbreeding and distant outbreeding may reduce fitness below the level of individuals with intermediate parental relatedness. In the haplodiploid plant-inhabiting predatory mite Phytoseiulus persimilis, which is patchily distributed within and among host plants, fitness is indeed reduced in the short term, i.e. by a single generation of inbreeding. However, in the medium to long term (multiple generations), distant out-breeding should provide for favorable demographic founder effects in isolated populations. We tested this prediction in isolated experimental lineages founded by females mated to a sibling (close inbreeding), a male from the same population (intermediate relatedness) or a male from another population (distant outbreeding) and monitored lineage growth and persistence over four generations. Cross-generationally, lineages founded by distantly outbred females performed the best, i.e. produced the most descendants. However, this was solely due to superior performance from the F2 generation onwards, whereas in the F1 generation, lineages founded by females mated to males from their own population (intermediate relatedness) performed the best, as predicted from short-term in- and out-breeding depression effects. At the genetic level, this result was most likely due to distantly outbred founders introducing higher allelic variability and lower homozygosity levels, counterbalancing inbreeding depression, which inevitably occurs in isolated lineages, from the F2 generation onwards.
Founder effects, i.e. effects emerging from founding of populations/lineages by a subset of individuals of the parental population, have decisive influence on the occurrence and intensity of inbreeding depression [1,2]. Founder effects change the genetic composition, usually by reducing variation, of daughter populations/lineages relative to the parental population and are thus especially relevant for inbreeding by organisms structured in small and fragmented or locally isolated populations with limited genetic exchange [3,4].
Mean abundance of predator lineages over the whole experimental period was significantly influenced by the interaction between founder inbreeding level and population origin (GEE: Wald χ22 = 6.402, P = 0.04), whereas neither founder inbreeding level (Wald χ22 = 2.749, P = 0.25) nor population origin (Wald χ12 = 0.281, P = 0.59) exerted significant main effects (Fig 3). Within either population origin, mean lineage abundance varied significantly with founder inbreeding level (GEE for Sicily: Wald χ22 = 7.683, P = 0.02; Greece: Wald χ22 = 6.319, P = 0.04). For the Sicily origin, lineages founded by sib-mated females reached significantly lower abundances (on average 20 to 30% lower) than lineages founded by females mated to males from the same population or to males from Greece (LSD: P < 0.05) (Fig 3). For the Greece origin, lineages founded by females mated to males from Sicily reached significantly higher abundances (on average 20% higher) than the population founded by females mated to males from the same population (LSD: P = 0.01) (Fig 3). All other pairwise comparisons were non-significant (P > 0.05). Two lineages founded by sib-mated females (one from Sicily and one from Greece) went extinct within the F1 generation (no individuals observed on day 15 and 20, respectively). All lineages founded by females mated to males from the same or the other population persisted until the end of the experiment.
Our study documents demographic founder effects in dependence of the founders’ in- and out-breeding status in the haplodiploid plant-inhabiting predatory mite P. persimilis. Trans-generationally, that is, over approximately four generations, closed lineages founded by distantly outbred females (mates coming from different populations) reached higher abundance levels than lineages founded by heavily (sibling mates) and lightly (mates coming from the same population) inbred females. However, time-dependent inter-lineage comparison revealed superior performance of lineages founded by outbred females only from the F2 generation onwards, whereas in the F1 generation lineages founded by females with intermediate mate relatedness levels (same population) performed better than lineages founded by sib-mated females and lineages founded by distantly outbred females (different populations).