Low levels of regional differentiation and little evidence for local adaptation in rare arable plants
Introduction
Arable plants are keystone species in arable landscapes fulfilling various provisioning, regulating and supporting ecosystem services (Fagúndez, 2015). In Central Europe, arable plants are natives or archaeophytes which have been part of the cultural landscapes since several thousands of years. Due to changes in agricultural management, including simplified crop rotations, frequent fertiliser and herbicide application, improved seed cleaning and the abandonment of marginal agricultural land, these species are rapidly declining and many have become very rare (Storkey et al., 2012). ‘Land-sharing’ strategies combine low-intensity crop production with the conservation of biodiversity and thus may contribute to the restoration of agrobiodiversity (Albrecht, Cambecèdes, Lang, & Wagner, 2016). As the spontaneous recovery of rare arable plant populations is unlikely due to depleted soil seed banks and an insufficient seed dispersal (Bischoff 2005), establishing these species by seed or soil transfer can be meaningful (Albrecht et al., 2016). Lang, Prestele, Wiesinger, Kollmann, & Albrecht (2016; 2018) found that a successful reintroduction increases the seed production and number of seeds in the soil without a significant reduction in crop yield under low-intensity farming.
The sowing of arable plants is a promising tool for the restoration of agrobiodiversity but requires careful selection of seed origin to avoid risks associated with the transfer of non-local genotypes, including maladaptation, cryptic invasion, outbreeding depression, and altered biotic interactions with associated organisms (Vander Mijnsbrugge, Bischoff, & Smith, 2010). To ensure restoration success, the use of autochthonous seed material is recommended, following the ‘regional admixture provenancing concept’ of seed transfer zones in Germany (Bucharova et al., 2019). These zones are delineated based on climatic and geomorphological patterns, with supportive evidence present for common grassland species (Durka et al., 2017). However, endangered species are excluded from this concept due to the presence of substantial heterogeneity of environmental parameters within zones to which specialised species with fragmented populations could be adapted at a smaller scale (Bucharova et al., 2019). Thus, in order to identify the optimal scale for the seed transfer of rare arable plants, knowledge about species-specific patterns of genetic differentiation and local adaptation is required.
A meta-analysis by (Leimu & Fischer 2008) on different ecosystems showed evidence for local adaptation in plants at 45–71% of the studied sites. The degree of local adaptation depends mainly on the relative strength of selection, drift, and gene flow (Kawecki & Ebert, 2004). While knowledge about genetic diversity and its spatial patterns is available for noxious weeds and a few model species, such as Arabidopsis thaliana, only few studies have focused on endangered arable plants (but see Brütting, Meyer, et al., 2012; Meyer et al., 2015), and none of these studies provided comparisons within and among seed zones.
Water availability is a critical factor in plant growth which strongly varies with climate and soil among sites. There are different strategies available for plants to cope with drought stress, including a higher tolerance based on increased root allocation, or avoidance by accelerated flowering for the more rapid completion of the life cycle. For several species, including annuals, intraspecific variation in response to drought was found, which resulted in a higher sensitivity to drought stress for provenances from humid regions in comparison with arid regions (e.g. Heschel, Sultan, Glover, & Sloan, 2004). Due to climate change, summer drought is expected to further increase in Central Europe, and drought adaptation might be increasingly important for arable plants (Rühl, Eckstein, Otte, & Donath, 2016).
Population differentiation can be investigated by population-genetic approaches using molecular markers, and by quantitative-genetic approaches using phenotypic traits (Savolainen, Lascoux, & Merilä, 2013). Molecular-genetic techniques usually measure neutral genetic variation that does not inform about selective processes. In contrast, quantitative-genetic analyses of phenotypic traits are more useful for studying adaptive evolution (Holderegger, Kamm, & Gugerli, 2006). For the latter approach the exclusion of non-genetic parental (mostly maternal) effects is required. This can be achieved by growing plants for at least one generation under standardised conditions (Bischoff & Müller-Schärer, 2010), and population differentiation can be afterwards tested on F2 generations in the greenhouse and common garden experiments. Since significant differences in phenotypic traits might be attributed to genetic drift or inbreeding, especially in the case of small populations with low genetic diversity, reciprocal transplant experiments are available to help detect local adaptation (Kawecki & Ebert, 2004). By comparing the overall performance of plants from multiple populations growing in sympatry (local) with plants growing in allopatry (non-local environments), patterns of local adaptation can be revealed (Bucharova et al., 2017). However, the detection of local adaptation may vary among traits related to germination, survival, biomass, reproduction, or phenology (Leimu & Fischer 2008). In the case of arable plants, beside biomass which is usually closely correlated to seed production, reproductive phenology can be considered to be of great importance since the life cycle has to be completed before harvest. There is evidence for intraspecific variability in plant phenology, e.g. an earlier flowering with the increase of latitude due to a shorter growing season (Kollmann & Bañuelos, 2004). Moreover, it was shown that local adaptation to the timing of land management can influence phenology (Völler, Bossdorf, Prati, & Auge, 2017). However, knowledge about trait differentiation and local adaptation in rare arable plants is presently scarce.
To test for intraspecific genetically based differentiation in rare arable plants, a greenhouse experiment was set up in South Germany with 4–12 source populations of Arnoseris minima, Consolida regalis, Cyanus segetum, Legousia speculum-veneris and Teesdalia nudicaulis, respectively. Reciprocal transplant experiments were conducted to test for local adaptation under field conditions to the northern or southern regions within three seed transfer zones. While population differentiation was tested across the whole study area, within and among seed zones, transplant experiments focused on local adaptation within zones to fulfil the minimum standard of regional seed transfer in Germany. Maternal effects were excluded by growing the F1 generation in a common environment in the greenhouse and using only F2 for analysis. The following questions were addressed:
- a)
Are there any differences among source populations in regard to phenology and biomass production?
- b)
Is population differentiation increased under drought stress?
- c)
Can a higher fitness (establishment and biomass production) be perceived for plants grown in sympatry in comparison with those grown in allopatry, indicating local adaptation?
Section snippets
Study species
The five annual study species are typical representatives of the endangered Central European segetal flora. They have similar life cycles and cover a broad spectrum in terms of site requirements, degree of threat, pollination and breeding system (Table 1). All study species are able to produce high numbers of seeds which can persist in the soil seed bank over several years (Schneider, Sukopp, & Sukopp, 1994).
Study area and seed collection sites
Seeds of the five species were collected from arable fields in Bavaria ranging between
Regional differentiation among source populations
In the greenhouse experiment with F2 plants, there was little evidence for genetic differentiation in phenotypic traits among the different source populations. A significant effect of source population on biomass was observed in C. regalis, but not in the other study species (Table 2). For C. regalis, significant differences occurred in the south of zone 11, without drought stress, between source population 8 (0.73 ± 0.04 g) and 9 (1.44 ± 0.15 g) (Fig. A.2, Table A.3). Moreover, C. segetum
Low genetic differentiation
No differentiation among populations in A. minima, T. nudicaulis, and L. speculum-veneris, and differentiation between only two out of the 12 source populations in C. regalis and C. segetum under controlled conditions in the greenhouse indicated low genetically based differentiation in biomass production. As this may also result from genetic drift or inbreeding, differentiation in C. regalis and C. segetum biomass does not per se indicate local adaptation (Kawecki & Ebert 2004). While genetic
Author contributions
HA and JK initiated the research project; ML, HA and JK designed and supervised the experiments; ML collected and analysed the data; all authors contributed to the manuscript .
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We would like to convey our special thanks to the Foundation ’Bayerische KulturLandStiftung’ for project cooperation. We are grateful to numerous students at the Chair of Restoration Ecology and to the project farmers for their great efforts that made the experiments possible.
Funding
The research project ‘Arable plants for Bavaria´s cultural landscape’ was funded by the Bavarian Nature Conservation Fund and the Landwirtschaftliche Rentenbank.
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