Combining an Ecological Experiment and a Genome Scan Show Idiosyncratic Responses to Salinity Stress in Local Populations of a Seaweed

Abstract

Climate change-related effects threaten species worldwide; within-species populations may react differently to climate-induced stress due to local adaptation and partial isolation, particularly in areas with steep environmental gradients. Populations of the marine foundation seaweed Fucus vesiculosus are established over a steep salinity gradient at the entrance of the brackish water in the Baltic Sea (NE Atlantic). First, we analyzed the genetic differentiation among populations using thousands of genetic markers. Second, we measured the physiological tolerance to reduced salinity, a predicted effect of climate change in the study area, by measuring growth, phlorotannin (defense compounds) content, and maximum photochemical yield in tissue of the same individuals exposed to both current and projected future salinities. Our results show that despite short geographic distances (max 100 km), most populations were genetically well separated. Furthermore, populations responded very differently to a salinity decrease of four practical salinity units (psu) corresponding to projected future salinity. At the high salinity end of the gradient, some populations maintained growth at the cost of reduced phlorotannin production. However, at the low salinity end, mortality increased and growth was strongly reduced in one population, while a second population from similar salinity instead maintained growth and phlorotannin production. Among genetic markers that appeared as outliers (showing more genetic differentiation than the majority of loci), we found that four were associated with genes that were potential candidates for being under selection. One of these, a calcium-binding protein gene, also showed a significant genotype-phenotype relationship in the population where this genetic marker was variable. We concluded that local selection pressure, genetic affinity, and possibly also population history could explain the very different responses to reduced salinity among these populations, despite being from the same geographic area. Our results highlight the importance of local perspective in the management of species.

Induction of Phlorotannins and Gene Expression in the Brown Macroalga Fucus vesiculosus in Response to the Herbivore Littorina littorea

“…The design of a set of primers (Table 1) was based on EST clones from cDNA libraries representing of desiccated F. vesiculosus and F. serratus [27], a F.vesiculosus genome [57] and a microarray study [25] accessible through GEO series accession number GSE47975 (http: //www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE47975, accessed on 20 February 2011). Relative gene expression was analyzed with LightCycler ® 480 software (Roche Diagnostics, Mannheim, Germany), using the 2ˆ-∆CT method by using as references genes tua (Alpha tubulin) and ef1α (Translation elongation factor 1 alpha) [27].…”

Climate Change Increases Susceptibility to Grazers in a Foundation Seaweed

“…Changes in global temperature are also predicted to alter evaporation and increase precipitation, with the net effect of decreasing salinity in coastal areas (Jenkins, 1999;Wentz et al, 2007). This has already occurred, for example in the Baltic Sea where the salinity in surface water has decreased by -0.005 to -0.014 psu per year from 1982 to 2016 (Liblik and Lips, 2019) and is projected to decrease by 4 psu at the entrance to the Baltic Sea before the end of the century (Eilola et al, 2009;Kinnby et al, 2020). Furthermore, the Baltic Sea area has already experienced a documented abnormal increase in temperature which averages 0.5-1 • C per decade (HELCOM, 2013).…”

“…Changes to multiple climate factors can cause tissue necrosis (reduced salinity and increased temperature, Takolander et al, 2017), reduce growth (reduced salinity and increased temperature, Rugiu et al, 2018) or mitigate the effects of changes to a single variable (increased temperature and elevated pCO 2 , Mensch et al, 2016). Moreover, growth responses to climate change have also been observed to vary over small geographic areas (Kinnby et al, 2020) and over seasons (Wahl et al, 2020).…”

“…Phlorotannins are a group of polyphenolic metabolites that can occur in high concentrations in brown seaweeds, especially in fucoids. These compounds have several functions, including UV protection and chemical defense against grazers (Pavia et al, 1997;Toth and Pavia, 2007), and have been experimentally shown in F. vesiculosus to decrease when exposed to lower salinity (Connan and Stengel, 2011b;Kinnby et al, 2020) and elevated pCO 2 (Kinnby et al, 2021). Climate change induced alterations in chemical defenses and overall biochemical composition of seaweed biomass can have consequences for ecological interactions such as grazing pressure on the seaweeds.…”

“…This study investigates individual and interactive effects of changes in temperature, salinity, and pCO 2 on F. vesiculosus, using a fully crossed experimental design. By exposing seaweeds to the projected changes in average salinity, temperature, and pCO 2 in the study area (-4 psu, +5 • C, and +700 µatm; Eilola et al, 2009;Solomon, 2007;Cornwall and Hurd, 2016;Kinnby et al, 2020) by year 2100 we assess the effects on growth of F. vesiculosus, measured as area, biochemical composition (tissue phlorotannin content, C:N ratio, and ∂ 13 C), as well as the susceptibility of the seaweed to a common grazer, the snail Littorina obtusata. We hypothesize that these three climate change factors will affect growth of the seaweeds, more specifically that we would see an enhanced growth under elevated pCO 2 but also that there would be antagonistic effects from different combinations of these climate variables.…”