1 INTRODUCTION
Populations of the same species that co-exist spatially over at least a part of their life-cycle (Futuyma & Mayer, 1980; Mallet, Meyer, Nosil, & Feder, 2009), have interested evolutionary ecologists for decades since they may represent the first steps of speciation (Maynard Smith, 1966; Via, 2001). Reproductive isolation between sympatric populations may arise from adaptations to ecological niches, even in the absence of migration barriers (Kawecki, 1996, 1997; Turelli, Barton, & Coyne, 2001). In biodiversity research and conservation management, sympatric populations represent genetic diversity below the species level that is important to identify and monitor. Such populations contribute to the portfolio effect in ecosystem stability (Schindler, Armstrong, & Reed, 2015; Schindler et al., 2010) and to genetic diversity recognized in international conservation policy, e.g. the Convention on Biological Diversity (www.cbd.int).
Sympatric populations have been documented in a wide range of taxa from insects to large mammals, in both terrestrial and aquatic environments, as well as in plants (Attard, Beheregaray, & Möller, 2016; Guo et al., 2018; Knutsen et al., 2018; Orlov et al., 2012; Ravinet et al., 2016; Schönswetter et al., 2007; Verspoor, Smith, Mannion, Hurst, & Price, 2018). Theoretically, they can represent a continuum of genomic divergence dependent on their evolutionary history with respect to degree of isolation over time (Roux et al., 2016). Empirically, different degrees of genetic divergence between sympatric populations have been reported, indicating different evolutionary backgrounds and degree of isolation (Lu & Bernatchez, 1999; Taylor, 1999).
In the vast majority of cases, sympatric populations have been detected because the populations differ phenotypically (Jorde, Andersson, Ryman, & Laikre, 2018). Sympatric populations can be referred to as “cryptic” when no obvious morphological divergence has been detected between the populations (Bickford et al., 2007) and where their detection has been based exclusively on genetic data (Andersson et al., 2017).
The first case of cryptic sympatry in salmonids was reported for brown trout (Salmo trutta ) in 1976 in the small twin mountain Lakes Bunnersjöarna in central Sweden where contrasting homozygosity at an allozyme locus (a lactate dehydrogenase locus denoted LDH-1 ) indicated the existence of two coexisting, genetically distinct groupings (Allendorf, Ryman, Stennek, & Ståhl, 1976; Ryman, Allendorf, & Ståhl, 1979). An additional 53 allozyme loci were screened and five of those supported the division while the remaining 48 were fixed (or nearly fixed) for the same allele in both demes resulting in the conclusion of the existence of reproductively isolated, sympatric populations with little genetic divergence (Ryman et al., 1979). Statistically significant body size differences between the two populations (denoted demes) were detected (Deme II fish smaller than those in Deme I) but it was not possible to classify fish to deme based on visual inspection (Ryman et al., 1979). Further, the allozymes indicated greater amounts of genetic variation in Deme I than in Deme II.
Salmonid fishes represent one of the organism groups that has been most extensively studied with respect to natural population genetic structure (Utter, 2004), and a recent review found over 130 cases of sympatric populations to have been identified world-wide in salmonid fishes; less than 10 of those cases were cryptic (Jorde et al., 2018). Most of these studies used few genetic markers and it remains unclear if genetic divergence in sympatry evolves primarily through reproductive isolation and genetic drift, or if divergent selection acting on a restricted part of the genome is the primary evolutionary mechanism for such structures.
In the present paper, we reanalyze samples from Lakes Bunnersjöarna and apply single nucleotide polymorphism (SNP) array analyses as well as whole-genome resequencing analyses based on a recent genome assembly for brown trout (https://www.ncbi.nlm.nih.gov/assembly/GCF_901001165.1) to test ifi ) the existence of two reproductively isolated demes in these tiny lakes is supported, and if so, ii ) what the genome-wide divergence between the demes is and iii ) whether the previously observed differences in amount of genetic variation in a few allozyme loci is a genome-wide phenomenon or limited to a small number of loci.