Population size affects fitness in alpine species
In general, populations of rare species tended to be smaller than populations of common species. This might increase their risk of local extinction due to environmental or demographic stochasticity (Lande 1993).
Overall, the significant positive relationships of seed number and total seed mass per fruit with population size (Fig. 2b and c) and the trend of higher germination rates in larger populations support our hypothesis of a positive relationship between population size and fitness in alpine species. Seed number is a strong indicator of plant fitness (Boyd et al. 2022) and limited seed availability is an important reproductive constraint for populations of alpine plant species (Lindgren et al. 2007; Frei et al. 2012). Germination and seedling establishment are difficult within the short reproductive season and exposed to adverse alpine conditions such as frosts or droughts (Kobiv 2018). It appears likely that populations with limited seed production and low germination rates are at higher risk of local extinction.
Different mechanisms could explain why plants of small populations produce fewer seeds. A reduced seed number can result from reduced pollination visitation, since small populations are less attractive for insects (Jennersten 1988; Agren 1996). This effect might be even stronger in alpine habitats, where insect activity is generally lower due to environmental constraints (Totland and Sottocornola 2001). Despite the absence of genetic variation and genetic differentiation data, small populations of our study species might suffer from reduced gene flow within and between populations, increased gene drift and inbreeding. This could translate into reduced individual fitness. It remains unknown whether biotic or genetic reasons (or both) explain the reduced seed number in small populations of our study species. Our results align with previous studies on lowland species, highlighting seed number as the fitness parameter most dependent on population size (Fischer and Matthies 1998; Morgan 1999). Nevertheless, experimental studies are required to understand the mechanisms underlying the relationship between population size and seed production.
We observed only positive but no negative relationships between plant fitness and population size, indicating that there might be no trade-off between seed quantity and quality in populations of our study species. While larger seeds are generally more robust under environmental stressors as for instance frost, drought or competition, smaller seeds can be produced in larger numbers with the same amount of resources (Bufford and Hulme 2021). According to Lázaro and Larrinaga (2018), trade-offs between seed quantity and quality are particularly strong in alpine species. Our results suggest that the extent to which such a trade-off is present in populations of alpine species might vary across species. However, we observed significantly lower seed mass in populations at higher elevations. This might be due to the short vegetation time, which can constrain seed mass by the short time available for seed provisioning (Baker 1972). As lower seed mass led to lower germination rates in our study species, reproduction might be limited at high elevations. This could put even more pressure on small populations that already suffer from reduced fitness.
We conclude that there is a positive relationship between population size and fitness in our study species. Therefore, small populations of these species might have an increased risk of local extinction. Moreover, large populations that experience a bottleneck due to droughts or increased competition could also fall into an extinction vortex.
Rare species do not have reduced individual fitness
Our data do not support the hypothesis that plants from rare species are less fit than plants from common species. Plants of G. alpina and P. nivea produced offspring with smaller size compared to the common G. acaulis and P. crantzii. This pattern can be explained on one hand by rarity, but on the other hand also by an adaptation of the plants of these species to high alpine habitats (Halbritter et al. 2018). Seed set and germination were even higher in rare than in common species, indicating that naturally rare species are well adapted to their environment. Therefore, our results support our alternative hypothesis that genetic load has been purged in populations of naturally rare species.
Beside the differences in seed set and germination, time to germination was significantly shorter among rare than among common species, but the variance explained by this model was very low (R2 m\(<\)0.1). Alpine species implement different germination strategies depending on the species habitat (Tudela-Isanta et al. 2018); hence, time to germination is may not provide an accurate estimate of plant fitness. Since G. alpina and P. nivea both occur at high alpine sites, the earlier onset of germination in these species could reflect adaptation to a very short vegetation time in high alpine habitats rather than an effect of rarity, per se. In addition, earlier germination is not necessarily advantageous, as drought or frost can threaten the seedlings. A more meaningful estimate of plant fitness might be the variation in time to germination. Germination is the most critical stage in a plant’s life cycle and plasticity in germination could play an important role in the response of alpine species to climate change (Paulů et al. 2017).
To conclude, our results do not confirm the very general observation of a reduced fitness and reduced survival in rare species (Boyd et al. 2022). Rather, they agree with Paulů et al. (2017), who studied 18 congeneric species pairs from central European mountains and did not find reduced individual fitness in rare species. Hence, naturally rare species might be well adapted to their environment and other reasons than low plant fitness must be responsible for their rarity.
In general, the assessment of purely short-term fitness traits is a limitation of not only this study but also many others. First, alpine plants reproduce with a high variability among years, due to aspects such as variation in snowmelt time (Kudo and Hirao 2006). Therefore, alpine species should be sampled over several years to obtain data that are more reliable. Second, an important long-term fitness parameter is the population’s ability to adapt to changing environmental conditions. In the context of climate change, it might be important to investigate the extent of adaptive trait plasticity (e.g. onset and duration of flowering and germination under different environmental conditions) as an indicator for adaptive capacity in alpine species.
Another limitation of our study is that the analysis of germination, time to germination, offspring survival and offspring size included only half of our study species, because the Androsace and Viola species germinated poorly (\(<\)0.5–10 %). Either the commonly known conditions needed to break seed dormancy for alpine species (cold stratification and moist-chilling, warm-cued germination and changing temperature and light conditions; Shimono and Kudo 2005; Fernández-Pascual et al. 2021) are unsuitable for these four species, or this result shows that half of our study species are mostly incapable of germination. Germination already failed in some other alpine species, regardless of the conditions (Shimono and Kudo 2005). However, this does not weaken our conclusion of a positive relationship between fitness and population size in alpine species. We still observed a positive relationship between germination and population size in the reduced dataset. In addition, we observed positive relationships between seed-related traits and population size across all eight species. For larger and elaborate germination experiments of alpine species, we strongly recommend small pilot studies in advance to define suitable germination conditions.
Relationships between population size and individual fitness are equally strong for rare and common alpine species
We hypothesised that rare species show stronger relationships between population size and fitness than common species. However, relationships between fitness and population size were equally strong in rare and common species. This again supports our alternative hypothesis that genetic load has been purged in populations of our rare study species.
On the species level, we found significant positive relationships between fitness and population size in the rare G. alpina and P. nivea and in the common A. chamaejasme and P.crantzii, indicating that an extinction vortex is ongoing in small populations of these species. Both Potentilla species form apomictic seeds (Hörandl et al. 2011; Nylehn et al. 2003), probably to speed up reproduction as an adaptation to short vegetation periods at high elevations (Schinkel et al. 2016). Genetic variability can be strongly reduced in small populations with a large proportion of apomicts (Adolfsson and Bengtsson 2007), which might explain the low plant fitness in small populations of our Potentilla species. Hence, negative effects of a small population size on individual fitness might depend on the reproductive strategy.
The fact that we did not observe significant relationships between population size and fitness on the species level in A. puberula, G. acaulis, V. lutea and V. calcarata does not mean that an extinction vortex is absent in small populations of these species. Otherwise, we would not have observed significant overall effects. It is likely that the relationship is simply weaker in these species and therefore not significant with limited statistical power.
Studies on non-alpine species found no significant difference between rare and common species; neither in the strength of the relationship between population size and fitness nor in population size per se (Leimu et al. 2006). Our results suggest that although naturally rare species tended to occur in smaller populations, the relationship between fitness and population size might be equally strong in naturally rare and in common alpine species. Consequently, populations of both rare and common alpine plant species may face the potential of entering an extinction vortex. The presence of an extinction vortex in alpine species could limit their ability to adapt and migrate, making them more susceptible to rapid environmental change. Hence, these species could be severely threatened by climate change, which is predicted to place high climatic and biotic pressure on alpine populations (Theurillat and Guisan 2001).