Demographic and genetic patterns of variation among populations of Arabidopsis thaliana from contrasting native environments

Abstract

Background: Understanding the relationship between environment and genetics requires the integration of knowledge on the demographic behavior of natural populations. However, the demographic performance and genetic composition of Arabidopsis thaliana populations in the species' native environments remain largely uncharacterized. This information, in combination with the advances on the study of gene function, will improve our understanding on the genetic mechanisms underlying adaptive evolution in A. thaliana.

Methodology/principal findings: We report the extent of environmental, demographic, and genetic variation among 10 A. thaliana populations from Mediterranean (coastal) and Pyrenean (montane) native environments in northeast Spain. Geographic, climatic, landscape, and soil data were compared. Demographic traits, including the dynamics of the soil seed bank and the attributes of aboveground individuals followed over a complete season, were also analyzed. Genetic data based on genome-wide SNP markers were used to describe genetic diversity, differentiation, and structure. Coastal and montane populations significantly differed in terms of environmental, demographic, and genetic characteristics. Montane populations, at higher altitude and farther from the sea, are exposed to colder winters and prolonged spring moisture compared to coastal populations. Montane populations showed stronger secondary seed dormancy, higher seedling/juvenile mortality in winter, and initiated flowering later than coastal populations. Montane and coastal regions were genetically differentiated, montane populations bearing lower genetic diversity than coastal ones. No significant isolation-by-distance pattern and no shared multilocus genotypes among populations were detected.

Conclusions/significance: Between-region variation in climatic patterns can account for differences in demographic traits, such as secondary seed dormancy, plant mortality, and recruitment, between coastal and montane A. thaliana populations. In addition, differences in plant mortality can partly account for differences in the genetic composition of coastal and montane populations. This study shows how the interplay between variation in environmental, demographic, and genetic parameters may operate in natural A. thaliana populations.

Figure 1. Geographic location of populations.

The map shows the location of A. thaliana populations of study in coastal (BAR, COC, HOR, MUR, and POB) and montane (ALE, BIS, PAL, VDM, and VIE) areas in NE Spain.

Figure 2. Photographs of study populations.

The photographs show the habitat type and the area where permanent plots were laid down. Left and right panels are montane and coastal populations, respectively. Populations are ranked according to their altitude within each region.

Figure 3. Climatic patterns for coastal and montane regions.

The three panels show mean (± SE) values of (A) monthly minimum temperature, (B) monthly maximum temperature, and (C) monthly total precipitation for montane (filled dots) and coastal (hollow cuadrats) populations.

Figure 4. Persistence and germination of seeds buried in the soil seed bank.

The two panels show mean (± SE) values of (A) percent seed mortality and (B) percent seed germination of the soil seed bank experiment conducted on montane (ALE, BIS, and PAL) and coastal (HOR, MUR and POB) A. thaliana populations. Seeds were collected and buried in local populations in spring 2007 and retrieved periodically every six months: autumn 2007, spring 2008, and autumn 2008.

Figure 5. Total number of plants per population over time.

The different panels show the number of plants per population and survey (October 2007, December 2007, March 2008, April 2008, and May 2008) for montane and coastal A. thaliana populations. Asterisks indicate that data were not available at HOR because the site was destroyed in late winter. Populations are ranked according to their altitude within each region.