The genetic basis for ecological adaptation of the Atlantic herring revealed by genome sequencing

Abstract

Ecological adaptation is of major relevance to speciation and sustainable population management, but the underlying genetic factors are typically hard to study in natural populations due to genetic differentiation caused by natural selection being confounded with genetic drift in subdivided populations. Here, we use whole genome population sequencing of Atlantic and Baltic herring to reveal the underlying genetic architecture at an unprecedented detailed resolution for both adaptation to a new niche environment and timing of reproduction. We identify almost 500 independent loci associated with a recent niche expansion from marine (Atlantic Ocean) to brackish waters (Baltic Sea), and more than 100 independent loci showing genetic differentiation between spring- and autumn-spawning populations irrespective of geographic origin. Our results show that both coding and non-coding changes contribute to adaptation. Haplotype blocks, often spanning multiple genes and maintained by selection, are associated with genetic differentiation.DOI: http://dx.doi.org/10.7554/eLife.12081.001

Spawning time of Atlantic herring ( Clupea harengus ) populations within a restricted area reflects their otolith growth at the larval stage

“…Spawning time and location of herring are affected by genetic factors (Martinez Barrio et al, 2016) supporting that NSS, CSS and Landvik herring might represent discrete populations. Even though no direct evidence for natal homing being essential for the discrete population concept exist in this thesis Paper II, there are some indications that fidelity of adult individuals to time and conditions of spawning resemble their own situation at the larval stage (Paper III).…”

“…This variety is, in theory, a good prerequisite when studying the population structure of herring, because genetic differentiation might arise based on isolation-by-distance (Wright, 1965) or environmental differences leading to phenotypic variation. Phenotypic differences of Atlantic herring have been well studied (see e.g., and recent studies also suggested genetic differentiation between populations Martinez Barrio et al, 2016). However, herring populations are often highly migratory and undertake long-distance migrations from a few 100 km to more than 1000 km between feeding, overwintering, and spawning areas.…”

“…The population structure of Atlantic herring has been a research topic since the end of the 19 th century (Heincke, 1898;Hjort, 1914). However, more than a century later, it is still debated how herring populations are spatially and temporally structured (Mariani et al, 2005;Reiss et al, 2009;Martinez Barrio et al, 2016). Within this single species, evidence exists for all three population concepts from spatial discrete populations , though metapopulations (McQuinn, 1997a), to a panmictic population (Smith and Jamieson, 1986;Ciannelli et al, 2013).…”

“…The attempt to identify and separate populations in this thesis was based on phenotypic traits and behavioral differences and not by using genetic markers. Basically, it can be expected that genetic methods should resolve the population structure of herring at the beginning of the 21 st century but despite the rapid development, from microsatellite DNA analyses (Mariani et al, 2005;Bekkevold et al, 2007) over single nucleotide polymorphism (SNP) analyses Limborg et al, 2012) to whole-genome sequencing (Martinez Barrio et al, 2016;Lami-chhaney et al, 2017), identification at individual levels is not yet possible. Altogether, further refinements of genetic analyses are necessary, and in combination with phenotypic traits, we might be able to identify and separate individual fish from a mixed herring fishery in the near future .…”

“…Further, salinity conditions not only influence phenotypes but are also a clear genetically structuring factor in population integrity (Nielsen et al, 2004;Bekkevold et al, 2007;Martinez Barrio et al, 2016). To answer the question of whether the environment, genetic differentiation or a combination of both is the driving factor for varying phenotypic traits, common garden experiments, as conducted in Paper V, are necessary (Swain and Foote, 1999).…”