Genetic causes and consequences of Brown trout migratory behaviour

Abstract

Salmonids are among the most famous and economically important migrating organisms, but unfortunately also often endangered because of multiple human activities. As many other salmonids, brown trout exhibits diverse life history types related to migration strategies. Resident brown trout stay in rivers for their entire life. In contrast, migratory trout undergo a physiological and morphological transformation called smoltification before leaving their natal rivers to enter either sea, lakes or larger river sections. While the phenotypic variation between resident and migratory ecotypes is well documented, little is known about the intraspecific genetic variation associated with these different life history strategies. For management and conservation purposes, understanding the mechanisms behind migratory behavior is a necessity. To investigate the genetic causes and consequences of the life-history dichotomy in brown trout, we used RAD-sequencing to obtain thousands of SNPs used in two distinct studies. First, we focused on the boreal River Koutajoki watershed to understand the genetic structuring of natural populations in relation to different life histories (Lemopoulos et al. 2018). We sampled eleven sites: three main stems (one with two sections) with migratory trout and seven tributaries with assumedly resident trout. We found that the genome-wide patterns associated with life-histories. Tributary fish represented isolated unique genomic patterns that most likely had arisen because of residency, and main stem fish were more admixed and had higher heterozygosity indicating history of migrations and occasional spawning in neighboring rivers. Second, we compared pairs of resident – migratory populations to identify potential candidate genes associated with migratory behavior. We focused on the Koutajoki watershed and complemented the study using populations from the River Oulujoki watershed. We combined different genome-scans approaches and found in total eight SNP outliers that associated with migratory behavior. We revealed, for the first time, candidate genes linked to life-history dichotomy in brown trout. Using the Atlantic salmon genome, we identified putative functions of these SNPs. Among them, we found genes involved in osmoregulation processes as well as cadherins, glutamates and zinc-fingers genes. These three gene families are involved in migratory behavior of other salmonids, indicating a potential common set of genes associated with salmonid migrations. Our results suggest that migratory behavior in brown trout plays a major evolutionary role in shaping natural populations. They also suggest that there is significant genetic basis for the migratory tendency in brown trout. These results bear significant implications for conservation: unintended mixing of resident and migratory fish due to stockings should be avoided, and migratory stocks must be conserved independently as there are no other stocks that could replace them when lost