Although it has become clear that sexual selection may shape mating systems and drive speciation, the potential constraints of environmental factors on processes and outcomes of sexual selection are largely unexplored. Here, we investigate the geographic variation of such environmental factors, more precisely the quality and quantity of nest resources (bivalve shells) along a salinity gradient in the Baltic Sea Area (Baltic Sea, Sounds and Belts, and Kattegat). We further test whether we find any salinity-associated morphological differences in body size between populations of common gobies Pomatoschistus microps, a small marine fish with a resource-based mating system. In a geographically expansive field study, we sampled 5 populations of P. microps occurring along the salinity gradient (decreasing from West to East) in the Baltic Sea Area over 3 consecutive years. Nest resource quantity and quality decreased from West to East, and a correlation between mussel size and male body size was detected. Population density, sex ratios, mating- and reproductive success as well as brood characteristics also differed between populations but with a less clear relation to salinity. With this field study we shed light on geographic variation of distinct environmental parameters possibly acting on population differentiation. We provide insights on relevant ecological variation, and draw attention to its importance in the framework of context-dependent plasticity of sexual selection.

Declines of large predatory fish due to overexploitation are restructuring food webs across the globe. It is now becoming evident that restoring these altered food webs requires addressing not only ecological processes, but evolutionary ones as well, because human-induced rapid evolution may in turn affect ecological dynamics. We studied the potential for niche differentiation between different plate armor phenotypes in a rapidly expanding population of a small prey fish, the three-spined stickleback (Gasterosteus aculeatus). In the central Baltic Sea, three-spined stickleback abundance has increased dramatically during the past decades. The increase in this typical mesopredator has restructured near-shore food webs, increased filamentous algal blooms, and threatens coastal biodiversity. Time-series data covering 22 years show that the increase coincides with a decline in the number of juvenile perch (Perca fluviatilis), the most abundant predator of stickleback along the coast. We investigated the distribution of different stickleback plate armor phenotypes depending on latitude, environmental conditions, predator and prey abundances, nutrients, and benthic production; and described the stomach content of the stickleback phenotypes using metabarcoding. We found two distinct lateral armor plate phenotypes of stickleback, incompletely and completely plated. The proportion of incompletely plated individuals increased with increasing benthic production and decreasing abundances of adult perch. Metabarcoding showed that the stomach content of the completely plated individuals more often contained invertebrate herbivores (amphipods) than the incompletely plated ones. Since armor plates are defense structures favored by natural selection in the presence of fish predators, the phenotype distribution suggests that a novel low-predation regime favors stickleback with less armor. Our results suggest that morphological differentiation of the three-spined stickleback has the potential to affect food web dynamics and influence the persistence and resilience of the stickleback take-over in the Baltic Sea.

The three-spined stickleback (Gasterosteus aculeatus) is an important model system for the study of parallel evolution in the wild, having repeatedly colonized and adapted to freshwater from the sea throughout the northern hemisphere. Previous studies identified numerous genomic regions showing consistent genetic differentiation between freshwater and marine ecotypes but these had typically limited geographic sampling and mostly focused on the Eastern Pacific region. We analysed population genomic data from global samples of the three-spined stickleback marine and freshwater ecotypes to detect loci involved in parallel evolution at different geographic scales. Most signatures of parallel evolution were unique to the Eastern Pacific and trans-oceanic marine-freshwater differentiation was restricted to a limited number of shared genomic regions, including three chromosomal inversions. On the basis of simulations and empirical data, we demonstrate that this could result from the stochastic loss of freshwater-adapted alleles during the invasion of the Atlantic basin and selection against freshwater-adapted variants in the sea, both of which can reduce standing genetic variation available for freshwater adaptation outside the Eastern Pacific region. Moreover, the elevated linkage disequilibrium associated with marine-freshwater differentiation in the Eastern Pacific is consistent with secondary contact between marine and freshwater populations that evolved in isolation from each other during past glacial periods. Thus, contrary to what earlier studies from the Eastern Pacific region have led us to believe, parallel marine-freshwater differentiation in sticklebacks is far less prevalent and pronounced in all other parts of the species global distribution range. Population genomic data from a global dataset of three-spined sticklebacks show that parallel signatures of marine to freshwater differentiation are less common than previously thought.

Human activity is altering the dynamics of populations through effects on fecundity, mortality and migration. An increased abundance of three-spined stickleback (Gasterosteus aculeatus) in the Baltic Sea has been attributed to a human-caused decline of top predators. However, recent research indicates that a top-down effect cannot fully explain the population growth, but the contribution of a bottom-up effect has not been investigated. Yet, anthropogenic eutrophication has increased algae biomass at the spawning sites of the stickleback and, thus, the abundance of benthic prey. We investigated if increased fecundity could have contributed to the population growth of the stickleback by analysing a two decade time series of stickleback abundance, fecundity, and body size at three spawning sites. The results show an increase in the proportion of gravid females in the populations, which correlates with the population growth. In particular, the proportion of gravid females late in the spawning season has increased, which indicates enhanced food intake at the sites during the spawning season. Thus, a bottom-up effect could have contributed to the growth of the populations by increasing the number of egg clutches females produce. These results stress the importance of considering both bottom-up and top-down processes when investigating the mechanisms behind human impact on population dynamics.

Heritable phenotypic differences between populations, caused by the selective effects of distinct environmental conditions, are of commonplace occurrence in nature. However, the actual genomic targets of this kind of selection are still poorly understood. We conducted a quantitative trait locus (QTL) mapping study to identify genomic regions responsible for morphometric differentiation between genetically and phenotypically divergent marine and freshwater nine-spined stickleback (Pungitius pungitius) populations. Using a dense panel of SNP-markers obtained by restriction site associated DNA sequencing of an F-2 recombinant cross, we found 22 QTL that explained 3.5-12.9% of phenotypic variance in the traits under investigation. We detected one fairly large-effect (PVE = 9.6%) QTL for caudal peduncle length-a trait with a well-established adaptive function showing clear differentiation among marine and freshwater populations. We also identified two large-effect QTL for lateral plate numbers, which are different from the lateral plate QTL reported in earlier studies of this and related species. Hence, apart from identifying several large-effect QTL in shape traits showing adaptive differentiation in response to different environmental conditions, the results suggest intra-and interspecific heterogeneity in the genomic basis of lateral plate number variation.

Novel physiological challenges in different environments can promote the evolution of divergent phenotypes, either through plastic or genetic changes. Environmental salinity serves as a key barrier to the distribution of nearly all aquatic organisms, and species diversification is likely to be enabled by adaptation to alternative osmotic environments. The threespine stickleback (Gasterosteus aculeatus) is a euryhaline species with populations found both in marine and freshwater environments. It has evolved both highly plastic and locally adapted phenotypes due to salinity-derived selection, but the physiological and genetic basis of adaptation to salinity is not fully understood. We integrated comparative cellular morphology of the kidney, a key organ for osmoregulation, and candidate gene expression to explore the underpinnings of evolved variation in osmotic plasticity within two populations of sticklebacks from distinct salinity zones in the Baltic Sea: the high salinity Kattegat, representative of the ancestral marine habitat; and the low salinity Bay of Bothnia. A common-garden experiment revealed that kidney morphology in the ancestral high-salinity population had a highly plastic response to salinity conditions whereas this plastic response was reduced in the low-salinity population. Candidate gene expression in kidney tissue revealed a similar pattern of population specific differences, with a higher degree of plasticity in the native high-salinity population. Together these results suggest that renal cellular morphology has become canalized to low salinity, and that these structural differences may have functional implications for osmoregulation.