Reduced fitness at early life stages in peripheral versus core populations of Swiss stone pine (Pinus cembra) is not reflected by levels of inbreeding in seed families

Abstract

Small and fragmented populations are prone to mating among related individuals, increasing homozygosity and likely negatively affecting offspring fitness. Such a trend may be enforced by environmental changes in species with narrow ecological niches because inbred populations are more prone to become maladapted as compared to outcrossed populations. Here, we studied differences in offspring fitness and inbreeding levels between core and peripheral populations of Swiss stone pine (Pinus cembra). We collected open-pollinated progenies of P. cembra in large, contiguous and in small, isolated populations (core vs. periphery). Seeds were germinated and grown in a common garden to test for differences in fitness parameters, whereas subsamples of seed lots were genotyped at seven nuclear microsatellites to calculate selfing rates. We found significantly lower seed production, higher embryo abortion rates and lower germination success in small peripheral compared to large core populations of P. cembra. In contrast, winter survival and first-year growth of seedlings did not significantly differ between the two population types. These results indicate higher inbreeding depression at the earliest life stages in small and fragmented populations compared to populations from the contiguous range of P. cembra. However, we found no correlation between any fitness parameters and progenyderived selfing rates. We explain this discrepancy by the fact that inbreeding depression mostly affects embryo abortion rates in Pinaceae. This cannot be genetically quantified because non-developed embryos cannot be genotyped. We infer that population fragmentation in the long term negatively affects natural regeneration in this long-lived, wind-pollinated conifer species.

Bayesian approach reveals confounding effects of population size and seasonality on outcrossing rates in a fragmented subalpine conifer

“…2) estimated in this study, we can infer that in the Tatras about 69 % pollen travels up to 1 km, while 31 % would be immigrating from at least 1 km. Thus, our results are in line with the findings based on the direct approach by Salzer (2011). They also correspond well with general knowledge that species with saccate pollen are characterized by great pollen dispersal potential (Schwendemann et al 2007).…”

“…Birds typically bury several seeds together (Tomback et al 1993), enabling the development of a family structure. In fact, strong spatial genetic structure was found in populations of P. cembra in the Swiss Alps (Salzer 2011), providing some support for this prediction. However, we cannot be sure that strong spatial genetic structure is also present in the study populations, where clumps of individuals due to seed caching seem to be relatively rare.…”

“…Using a parentage assignment approach, Salzer (2011) revealed that within a marginal stand of P. cembra in the Alps, effective pollen dispersal distance was, depending on the conditions, <200 m or about 315 m on average (maximum distance of 659 m). Our own analysis revealed that the total pollen dispersal follows a heavy-tailed dispersal kernel, confirming great potential of P. cembra to long-distance pollen dispersal.…”

“…The spatial genetic structure within populations of P. cembra can show aggregation of genetically related individuals as a result of caching behavior of the nutcracker. Kin-structured regeneration can potentially fosters mating among relatives (Salzer 2011). Moreover, flowering and seed production in Swiss stone pine occurs every 2-3 years, but only a single year of 4-10 is an abundant mast year (Ulber et al 2004).…”

No reduction in genetic diversity of Swiss stone pine (Pinus cembra L.) in Tatra Mountains despite high fragmentation and small population size

“…However, Salzer and Gugerli (2012) inferred that in P. cembra, inbreeding depression is expressed mainly at the prezygotic and/or early embryonic phase by l mean of the prior distribution for h; 95 % credible intervals are given in parentheses; p-probability from one-tailed Wilcoxon signed-rank test of population bottlenecks; H e -H eq -the fraction of loci with Hardy-Weinberg expected heterozygosity greater than mutation-drift equilibrium heterozygosity; *test significant at the level 0.01; **test significant at the level 0.001 Our results clearly indicate that inbreeding is present in Swiss stone pine. Both sources of inbreeding (selfing and mating among relatives) were noted earlier in P. cembra populations (Lewandowski and Burczyk 2000;Politov et al 2008;Salzer and Gugerli 2012). In fragmented and isolated populations, where selfing and mating among relatives allow escape from pollen limitation, their benefits come at the cost of inbreeding depression.…”