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Ecol Evol
2022 May 20;125:e8868. doi: 10.1002/ece3.8868.
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An environmental gradient dominates ecological and genetic differentiation of marine invertebrates between the North and Baltic Sea.
Geburzi JC
,
Heuer N
,
Homberger L
,
Kabus J
,
Moesges Z
,
Ovenbeck K
,
Brandis D
,
Ewers C
.
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Environmental gradients have emerged as important barriers to structuring populations and species distributions. We set out to test whether the strong salinity gradient from the marine North Sea to the brackish Baltic Sea in northern Europe represents an ecological and genetic break, and to identify life history traits that correlate with the strength of this break. We accumulated mitochondrial cytochrome oxidase subunit 1 sequence data, and data on the distribution, salinity tolerance, and life history for 28 species belonging to the Cnidaria, Crustacea, Echinodermata, Mollusca, Polychaeta, and Gastrotricha. We included seven non-native species covering a broad range of times since introduction, in order to gain insight into the pace of adaptation and differentiation. We calculated measures of genetic diversity and differentiation across the environmental gradient, coalescent times, and migration rates between North and Baltic Sea populations, and analyzed correlations between genetic and life history data. The majority of investigated species is either genetically differentiated and/or adapted to the lower salinity conditions of the Baltic Sea. Species exhibiting population structure have a range of patterns of genetic diversity in comparison with the North Sea, from lower in the Baltic Sea to higher in the Baltic Sea, or equally diverse in North and Baltic Sea. Two of the non-native species showed signs of genetic differentiation, their times since introduction to the Baltic Sea being about 80 and >700 years, respectively. Our results indicate that the transition from North Sea to Baltic Sea represents a genetic and ecological break: The diversity of genetic patterns points toward independent trajectories in the Baltic compared with the North Sea, and ecological differences with regard to salinity tolerance are common. The North Sea-Baltic Sea region provides a unique setting to study evolutionary adaptation during colonization processes at different stages by jointly considering native and non-native species.
FIGURE 1. Map of the North Sea–Baltic Sea salinity gradient, showing the decadal interpolated average salinity from 2006 to 2015. Skagerrak, Kattegat, and Belt Sea comprise the transition zone between the North and Baltic Seas, that is, the area between the solid red lines. Salinity data from Hinrichs and Gouretski (2019) available at https://www.cen.uni‐hamburg.de/icdc/data/ocean/bnsc‐hyd.html
FIGURE 2. Haplotype networks for all 28 investigated species grouped by taxonomic affinity. Size of the circles is relative to the sample size, but not the same between species. Colors of the circles denote populations: black = North Sea, white = Baltic Sea, and asterisks denote non‐native species. Background colors distinguish between higher taxa. Overall sample size n in parentheses
FIGURE 3. Salinity tolerances and eastern distribution limit in the Baltic Sea of the investigated species. Dotted lines indicate enhanced low‐salinity tolerance in Baltic Sea populations in species where Baltic Sea‐specific salinity tolerance data were available. Bar colors indicate the higher taxonomic group of each species (compare Figure 2), and asterisks denote non‐native species. For species abbreviations, see Table 1
FIGURE 4. Population genetic rarefaction results for all species with more than 20 sequences per population. Red dots represent the point estimate based on the full dataset; gray violin plots, the distribution of estimates based on five random sequences per population; and black violin plots the distribution of estimates based on 10 random sequences. Asterisks denote non‐native species
FIGURE 5. Population genetic comparison of North and Baltic Sea populations of marine invertebrates. (a) Haplotype diversity and (b) nucleotide diversity. Black: more diverse in North Sea, white: more diverse in Baltic Sea, and gray: equally diverse. (c) Comparison between the differentiation indices Φ
ST and Jost's D, (d) comparison between the differentiation indices Φ
ST and Hudson's Snn. Black: significantly differentiated with both indices, gray: only differentiated with Jost's D (c) or Hudson's Snn (d), and white: undifferentiated with either index. For species abbreviations, see Table 1
FIGURE 6. Distribution of posterior probabilities for mutation‐rate scaled population size q for species with more than 20 sequences per population and distinct population differentiation. The maximal values displayed for q denote the upper bounds of the uniform prior. The distribution of the Baltic Sea population is shown as a gray line; the distribution of the North Sea population, as a black line; and the distribution of the ancestral population, as a dashed line
FIGURE 7. Distribution of posterior probabilities for mutation‐rate scaled population size q for species with more than 20 sequences per population and distinct population differentiation. The maximal values displayed for q denote the upper bounds of the uniform prior. The distribution of the Baltic Sea population is shown as a gray line, and the distribution of the North Sea population as a black line
FIGURE 8. Correlations of pelagic larval duration (PLD) with ecological and genetic variables. (a) Genetic differentiation vs PLD, colors indicate adult mobility. (b) Easternmost longitude (which correlates strongly with salinity; see Figure 1) vs PLD, colors indicate higher taxonomic affinity
FIGURE 9. Ecological–genetic summary relevant to assess the potential of the North Sea–Baltic Sea transition zone as an ecological–genetic barrier. Left: nucleotide diversity ratio between Baltic Sea and North Sea populations; black bars indicate significant differences between Baltic and North Sea nucleotide diversity. Center: genetic differentiation (Φ
ST) between Baltic Sea and North Sea populations; black bars indicate significant differentiation. Right: salinity tolerance; dotted bars indicate a lower salinity tolerance limit in Baltic Sea populations; a superscripted “L” indicates that this was only shown for the larvae. Colors indicate higher taxonomic groups (compare Figure 2), and asterisks indicate non‐native species
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