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Adaptation to Low Salinity Promotes Genomic Divergence in Atlantic Cod (Gadus morhua L.).

Berg PR, Jentoft S, Star B, Ring KH, Knutsen H, Lien S, Jakobsen KS, André C - Genome Biol Evol (2015)

Bottom Line: Our results show that discrete regions within the Atlantic cod genome are subject to directional selection and associated with adaptation to the local environmental conditions in the Baltic- and the North Sea, indicating divergence hitchhiking and the presence of genomic islands of divergence.We report a suite of outlier single nucleotide polymorphisms within or closely located to genes associated with osmoregulation, as well as genes known to play important roles in the hydration and development of oocytes.Hence, our data suggest that adaptive responses to the environmental conditions in the Baltic Sea may contribute to a strong and effective reproductive barrier, and that Baltic cod can be viewed as an example of ongoing speciation.

View Article: PubMed Central - PubMed

Affiliation: Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Norway.

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Sampling locations of Atlantic cod specimens. Samples were obtained between 2002 and 2008 using trawl. Only mature specimens were selected for genetic analysis. See table 1 for a detailed description of the samples. Average surface salinity is denoted in ‰.
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evv093-F1: Sampling locations of Atlantic cod specimens. Samples were obtained between 2002 and 2008 using trawl. Only mature specimens were selected for genetic analysis. See table 1 for a detailed description of the samples. Average surface salinity is denoted in ‰.

Mentions: The Baltic Sea is one of the world’s largest semienclosed brackish seas, originating approximately 8,000 years ago (Zillén et al. 2008). Since then, the Baltic Sea has been colonized by both freshwater and marine teleosts (Ojaveer and Kalejs 2005). Limited water exchange and almost no tidal flow allow for stable salinity conditions, ranging from nearly fresh water in the northern Baltic Sea to around 30‰ at the border to the North Sea (fig. 1). Fossil records suggest that all contemporary marine teleost fish species have descended from a freshwater ancestry (Romer and Grove 1935; Griffith 1994; Long 1995; Fyhn et al. 1999), reflected by their hypo-osmotic state at the adult stage and their eggs and sperm in seawater (Griffith 1987; Fyhn et al. 1999; Finn and Kristoffersen 2007). The adaptation of neutral egg buoyancy toward those salinity levels found in the marine environment could arguably impede the successful colonization of less saline environments, as hyper-osmotic eggs would sink to the bottom, requiring an even higher degree of oocyte hydration, which is the case for Atlantic cod adapted to the Baltic environment (Nissling et al. 1994). Despite such considerations, some marine fishes with pelagic eggs, such as sprat, plaice and Atlantic cod, have colonized and successfully reproduce in low saline waters such as the Baltic Sea. Indeed, Atlantic cod colonized the central Baltic Sea some 8–6,000 YBP (Schmölcke 2006) when the surface salinity was 12–14‰. Since then, surface salinity has gradually decreased to around 7‰ today and around 14‰ at the spawning depth for Atlantic cod (50–100 m; Ignatius et al. 1981). Hence, the selection pressure to adapt to the low saline waters is a major force influencing the spawning success of cod in the Baltic Sea (Westin and Nissling 1991; Nissling et al. 1994), limited by factors such as egg buoyancy, sperm motility, and general osmoregulation. Importantly, Baltic cod spawns in a different season, compared with the North Sea and Western Baltic cod stocks, likely promoting reproductive isolation (Brander 1993; Wieland 2000; Brander 2005). The adaptation of Atlantic cod to low saline conditions is thus likely of relatively recent evolutionary origin, even though we cannot exclude the possibility that the founders of the Baltic population were already adapted to low salinity. This provides an excellent opportunity to study the genomic architecture behind salinity adaptation in a natural environment. As the ecological adaptation of Atlantic cod to a low-saline environment may contribute to reduced gene flow and thereby promote population divergence (cf. Nosil 2012), investigation of the genomic architecture of Baltic cod may give insights into ecological speciation in nature, and especially the genetic link between adaptation and reproductive isolation (cf. Seehausen et al. 2014).Fig. 1.—


Adaptation to Low Salinity Promotes Genomic Divergence in Atlantic Cod (Gadus morhua L.).

Berg PR, Jentoft S, Star B, Ring KH, Knutsen H, Lien S, Jakobsen KS, André C - Genome Biol Evol (2015)

Sampling locations of Atlantic cod specimens. Samples were obtained between 2002 and 2008 using trawl. Only mature specimens were selected for genetic analysis. See table 1 for a detailed description of the samples. Average surface salinity is denoted in ‰.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4494048&req=5

evv093-F1: Sampling locations of Atlantic cod specimens. Samples were obtained between 2002 and 2008 using trawl. Only mature specimens were selected for genetic analysis. See table 1 for a detailed description of the samples. Average surface salinity is denoted in ‰.
Mentions: The Baltic Sea is one of the world’s largest semienclosed brackish seas, originating approximately 8,000 years ago (Zillén et al. 2008). Since then, the Baltic Sea has been colonized by both freshwater and marine teleosts (Ojaveer and Kalejs 2005). Limited water exchange and almost no tidal flow allow for stable salinity conditions, ranging from nearly fresh water in the northern Baltic Sea to around 30‰ at the border to the North Sea (fig. 1). Fossil records suggest that all contemporary marine teleost fish species have descended from a freshwater ancestry (Romer and Grove 1935; Griffith 1994; Long 1995; Fyhn et al. 1999), reflected by their hypo-osmotic state at the adult stage and their eggs and sperm in seawater (Griffith 1987; Fyhn et al. 1999; Finn and Kristoffersen 2007). The adaptation of neutral egg buoyancy toward those salinity levels found in the marine environment could arguably impede the successful colonization of less saline environments, as hyper-osmotic eggs would sink to the bottom, requiring an even higher degree of oocyte hydration, which is the case for Atlantic cod adapted to the Baltic environment (Nissling et al. 1994). Despite such considerations, some marine fishes with pelagic eggs, such as sprat, plaice and Atlantic cod, have colonized and successfully reproduce in low saline waters such as the Baltic Sea. Indeed, Atlantic cod colonized the central Baltic Sea some 8–6,000 YBP (Schmölcke 2006) when the surface salinity was 12–14‰. Since then, surface salinity has gradually decreased to around 7‰ today and around 14‰ at the spawning depth for Atlantic cod (50–100 m; Ignatius et al. 1981). Hence, the selection pressure to adapt to the low saline waters is a major force influencing the spawning success of cod in the Baltic Sea (Westin and Nissling 1991; Nissling et al. 1994), limited by factors such as egg buoyancy, sperm motility, and general osmoregulation. Importantly, Baltic cod spawns in a different season, compared with the North Sea and Western Baltic cod stocks, likely promoting reproductive isolation (Brander 1993; Wieland 2000; Brander 2005). The adaptation of Atlantic cod to low saline conditions is thus likely of relatively recent evolutionary origin, even though we cannot exclude the possibility that the founders of the Baltic population were already adapted to low salinity. This provides an excellent opportunity to study the genomic architecture behind salinity adaptation in a natural environment. As the ecological adaptation of Atlantic cod to a low-saline environment may contribute to reduced gene flow and thereby promote population divergence (cf. Nosil 2012), investigation of the genomic architecture of Baltic cod may give insights into ecological speciation in nature, and especially the genetic link between adaptation and reproductive isolation (cf. Seehausen et al. 2014).Fig. 1.—

Bottom Line: Our results show that discrete regions within the Atlantic cod genome are subject to directional selection and associated with adaptation to the local environmental conditions in the Baltic- and the North Sea, indicating divergence hitchhiking and the presence of genomic islands of divergence.We report a suite of outlier single nucleotide polymorphisms within or closely located to genes associated with osmoregulation, as well as genes known to play important roles in the hydration and development of oocytes.Hence, our data suggest that adaptive responses to the environmental conditions in the Baltic Sea may contribute to a strong and effective reproductive barrier, and that Baltic cod can be viewed as an example of ongoing speciation.

View Article: PubMed Central - PubMed

Affiliation: Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Norway.

Show MeSH