Discussion
This study has shown that across three different seed production
environments, Fennoscandian and Italian Arabidopsis thalianapopulations differ consistently in seed dormancy. As expected from
differences in summer temperature and precipitation, Italian populations
produced seeds with stronger dormancy than did Fennoscandian
populations. In addition, we found wide variation in dormancy among
populations within each of the two geographic regions, and that for most
populations seed maturation environment had a strong effect on seed
dormancy. Below we discuss the results in relation to previous studies
documenting variation in seed dormancy among and within geographic
regions, effects of seed maturation environment on dormancy level, and
processes affecting population differentiation in this trait.
The stronger dormancy of seeds produced by Italian compared to
Fennoscandian populations is in accordance with expectations based on
climatic differences between the two regions. In the Italian populations
sampled, seed maturation in late April is followed by a long, hot and
dry summer, during which germination in response to occasional rain is
bound to be associated with high seedling mortality. By comparison, the
length of the period after seed maturation that is unfavourable for
seedling establishment is markedly shorter in Fennoscandian populations.
As a result, selection is expected to favour stronger primary seed
dormancy in the Italian compared to the Fennoscandian populations (cf.
Postma & Ågren, 2016). In experiments conducted at the two field sites,
August was identified as the optimal time of germination at the Swedish
site (Akiyama and Ågren 2014), and November at the Italian site
(Zacchello et al. 2020). The difference in seed dormancy between
Italian and Fennoscandian populations documented in the present study is
consistent with previous observations indicating a decrease in seed
dormancy with increasing latitude of origin among A. thalianaaccessions sampled across Europe (Kronholm et al. 2012; Debieuet al. 2013), and is likely to be representative for differences
between north European populations and southern populations at low
altitude in general.
Seed dormancy was strongly affected not only by the region of origin but
also by the maternal environment. Seed dormancy after 12 weeks of
after-ripening was stronger among seeds produced at the Swedish field
site than among seeds produced at the Italian field site, which is
consistent with differences observed in a former study documenting seed
dormancy of a population of recombinant inbred lines (RILs) planted at
the two sites and in the greenhouse (Postma and Ågren, 2015).
Differences in temperature during seed maturation may have contributed
to the observed difference in seed dormancy between the two field sites.
Low temperature during seed maturation has been found to increase seed
dormancy of A. thaliana (Chiang et al. 2011; Footittet al. 2011, 2013; Kendall and Penfield 2012; He et al.2014; Coughlan et al. 2017; Kerdaffrec and Nordborg 2017), but
also in a wide range of other species including Avena fatua ,Beta vulgaris , Chenopodium bonus-henricus , andPlantago lanceolata (see review Fenner 2018). During the two
months preceding seed dispersal (i.e., March and April in Italy, and May
and June in Sweden), air temperature was 1.5 ˚C colder in Sweden than in
Italy (Italy: 12.7˚C; Sweden: 11.2˚C; data recorded at the sites using
loggers as in Ågren & Schemske, 2012).
More surprising was the low germinability of seeds 12 weeks after
harvest in the greenhouse (Fig. 3 ). Because temperature in the
greenhouse was higher than at the field sites during seed maturation, we
expected seeds produced in the greenhouse to have the lowest dormancy,
as observed in the experiment with the RIL population (Postma and Ågren
2015). The present results indicate that environmental effects on
development of seed dormancy may vary among experiments also in a
greenhouse with a rather well-controlled temperature regime. Further
studies are needed to examine the possible influence of differences in
soil nutrient concentrations (Baskin and Baskin 2014) and water content
(Alboresi et al. 2005) for seed dormancy development in this
environment.
Correlations between germination proportions and measures of climate at
sites of origin were generally weak, and statistically significant only
for seeds produced by Fennoscandian populations in the greenhouse
(Table 4 ). One and three weeks after maturation, seed dormancy
tended to be negatively related to precipitation and positively related
to summer temperature at the sites of origin (Table 3 and 4 ). These
correlations are in line with predictions, and with associations between
seed dormancy and climate observed within the Iberic peninsula (Vidigalet al. 2016), and at a larger scale across Europe (Kronholmet al. 2012). In contrast to correlations documented for the
Fennoscandian populations, primary seed dormancy increased from sites
characterized by high temperature and wet conditions to those
characterized by lower temperature and dryer conditions among A.
thaliana populations sampled along an altitudinal gradient in
north-eastern Spain (Montesinos-Navarro et al., 2012). The
contrasting results show that correlations between seed dormancy and
climatic variables vary among regions, and suggest that the strength and
direction of correlations with different climatic variables will depend
on which part of the overall climatic variation is examined.
There are several possible reasons for the generally weak correlations
between primary seed dormancy and large-scale climatic variation within
regions, and the lack of statistically significant associations for
Italian populations. First, more populations were sampled in
Fennoscandia and the climatic range represented by these populations was
wider than that represented by the Italian populations (Table
S2 ), which should increase the chance of detecting relationships
between seed dormancy and environmental variables. Second, lower
survival and fecundity in the field compared to the greenhouse resulted
in smaller sample sizes, which should have reduced precision of
estimates and statistical power in analyses of variation in dormancy
among seeds matured in the field. Third, large-scale climatic data may
not well represent local microclimate since the latter is strongly
influenced by topography and exposure. For example, most of the
northernmost populations grow on steep, south-facing slopes, which
represent particularly warm and dry habitats in the landscape. Fourth,
in addition to micro-climatic conditions, optimal germination time and
seed dormancy may depend on environmental factors, such as soil
composition, which affects water-holding capacity, and on vegetation
cover, which affects intensity of competitive interactions. Fifth, seed
dormancy of present-day populations may not mirror optimal seed dormancy
at the sites of origin, but rather reflect founder events or genetic
correlations with traits more strongly related to fitness. This may seem
less likely considering the strong effects of germination date for
likelihood of seedling establishment, survival and fecundity in A.
thaliana (e.g., Donohue et al., 2005; Akiyama & Ågren, 2014; Postma &
Ågren, 2016; Zacchello et al., 2020). However, germination date is
determined not only by dormancy at the time of seed maturation, but also
by processes affected by the post-dispersal environment, such as rate at
which dormancy is released, and possible acquirement of secondary
dormancy (Montesinos et al., 2012; Postma et al., 2016; Martínez-Berdeja
et al., 2020). To further explore the consequences of the documented
variation in primary dormancy, it would be of interest to compare
dormancy release under contrasting field conditions and examine whether
any genotype × field environment interaction can be detected in this
trait, since this should influence the realized germination time.
In conclusion, this study has documented strong differentiation in seed
dormancy between Fennoscandian and Italian populations of A.
thaliana, but also among populations within each of the two regions.
The wide variation in seed dormancy documented among populations within
the two geographic regions indicates considerable evolutionary
flexibility, and is consistent with strong divergent selection on this
trait. Within Fennoscandia, which was the best sampled region, we found
an association between seed dormancy and temperature and precipitation,
two climatic factors that are expected to change in the future
(Masson-Delmotte et al. 2018). Reciprocal seed and seedling
transplants could be used to determine whether this among-population
differentiation in seed dormancy contributes to local adaptation.
Moreover, to assess the potential for adaptive evolution in response to
ongoing changes in climate, future studies should examine the extent to
which seed dormancy varies genetically within natural populations, and
whether current gene flow among divergent populations is sufficient to
maintain such variation.