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.