Genetically-based adaptive trait shifts at an expanding mangrove range margin

Many species are expanding beyond their distributional range margins in response to a warming planet. Due to marginal environmental conditions and novel selection pressures, range margins may foster unique genetic adaptations that can better enable species to thrive under the extreme climatic conditions at and beyond their current distributional limits. Neotropical black mangrove (Avicennia germinans) is expanding poleward into temperate salt marsh along Atlantic Florida, USA, with field evidence of adaptive trait shifts within range-margin A. germinans populations. However, whether these adaptive shifts have a genetic basis remains to be answered. We monitored twenty A. germinans maternal cohorts from areas in both the Atlantic Florida range core and margin in a greenhouse common garden with annual temperatures analogous to range-margin conditions. We measured variation in a series of phenotypic traits starting at initial planting of field-collected propagules and continuing until two years development. Maternal cohorts from the Atlantic Florida range margin consistently outperformed those from the range core throughout the experiment. Range-margin cohorts survived in greater numbers, established faster, and were less stressed under winter chilling and sub-zero temperatures that are often reached at the Atlantic range margin, but not within the range core. Range-margin cohorts did not grow taller, but instead invested more into lateral growth and biomass accumulation that presumably reflects adaptation to their colder and open canopy environment. Range-margin cohorts also exhibited leaf traits consistent with greater resource acquisition that may compensate for a shorter growing season and reduced light quality at higher latitude. Synthesis: We confirmed that there is a genetic basis to adaptive trait shifts towards an expanding mangrove range margin. Our results suggest that genetically-based phenotypic differences better enable these range-margin mangroves to thrive within their stressful environment and may facilitate further poleward expansion in the future. In addition, our documentation of adaptive trait variation among maternal cohorts of an ecologically-important mangrove foundation species, quantitative data that is lacking for mangroves, should help inform mangrove restoration initiatives.

Southern introgression increases adaptive immune gene variability in northern range margin populations of Fire-bellied toad

Northern range margin populations of the European fire-bellied toad (Bombina bombina) have rapidly declined during recent decades. Extensive agricultural land use has fragmented the landscape, leading to habitat disruption and loss, as well as eutrophication of ponds. In Northern Germany (Schleswig-Holstein) and Southern Sweden, this decline resulted in decreased gene flow from surrounding populations, low genetic diversity, and a putative reduction in adaptive potential, leaving populations vulnerable to future environmental and climatic changes. Previous studies using mitochondrial control region and nuclear transcriptome-wide SNP data detected introgressive hybridization in multiple northern B. bombina populations after presumed illegal release of toads from Austria. Here, we determine the impact of this introgression by comparing the body conditions (as a proxy for fitness) of introgressed and non-introgressed populations, and the genetic consequences in two candidate genes for putative local adaptation (the MHC II gene as part of the adaptive immune system and the stress response gene HSP70 kDa). We detected regional differences in body condition. We observed significantly elevated levels of within individual MHC allele counts in introgressed Swedish populations, associated with a tendency towards higher body weight, relative to regional non-introgressed populations. These differences were not observed among introgressed and non-introgressed German populations. Genetic diversity in both MHC and HSP was generally lower in northern than southern populations. Our study sheds light on the potential benefits of translocations of more distantly related conspecifics as a means to increase adaptive genetic variability and fitness of struggling range margin populations without distortion of local adaptation.

Drought sensitivity of Empetrum nigrum shrub growth at the species’ southern lowland distribution range margin

The ongoing warming of the Earth’s atmosphere is projected to cause a northward shift of species’ distributions, as they track their climatic optimum. In the rapidly warming Arctic, this has already led to an increase of shrubs in tundra ecosystems. While this northern expansion of woody biomass has been studied relatively extensively over the last decade, little research has been devoted to shrub growth responses at the southern margins of Northern Hemisphere shrubs. Here, we studied shoot length growth, its responses to climate over the period 2010–2017, and differences in leaf C and N content of the evergreen dwarf shrub Empetrum nigrum, as well as the vegetation composition and soil parameters at four sites located along a gradient of increasing dune age on the island Spiekeroog, northern Germany. The sites are located in the tri-national UNESCO world heritage site, the Wadden Sea. E. nigrum has a predominantly circum-arctic-boreal distribution and its southern distribution margin in European lowlands runs through northern Germany, where it is retreating northwards. We found a negative response to autumn (surface) temperatures and previous summer surface temperatures and/or a positive response to summer precipitation of E. nigrum growth, except at the oldest dune with the strongest E. nigrum dominance. Growth rates and plant species diversity declined with dune age. Our results suggest that E. nigrum growth is drought sensitive at its European southern range margin. We hypothesize that this sensitivity may form the basis for its northward retreat, which is supported by recent observations of E. nigrum dieback in Germany after the extreme drought in 2018 and model projections.