Investigating the genetic basis of vertebrate dispersal combining RNA‐seq, RAD‐seq and quantitative genetics

Abstract

Although animal dispersal is known to play key roles in ecological and evolutionary processes such as colonization, population extinction and local adaptation, little is known about its genetic basis, particularly in vertebrates. Untapping the genetic basis of dispersal should deepen our understanding of how dispersal behaviour evolves, the molecular mechanisms that regulate it and link it to other phenotypic aspects in order to form the so‐called dispersal syndromes. Here, we comprehensively combined quantitative genetics, genome‐wide sequencing and transcriptome sequencing to investigate the genetic basis of natal dispersal in a known ecological and evolutionary model of vertebrate dispersal: the common lizard, Zootoca vivipara. Our study supports the heritability of dispersal in semi‐natural populations, with less variation attributable to maternal and natal environment effects. In addition, we found an association between natal dispersal and both variation in the carbonic anhydrase (CA10) gene, and in the expression of several genes (TGFB2, SLC6A4, NOS1) involved in central nervous system functioning. These findings suggest that neurotransmitters (serotonin and nitric oxide) are involved in the regulation of dispersal and shaping dispersal syndromes. Several genes from the circadian clock (CRY2, KCTD21) were also differentially expressed between disperser and resident lizards, supporting that the circadian rhythm, known to be involved in long‐distance migration in other taxa, might affect dispersal as well. Since neuronal and circadian pathways are relatively well conserved across vertebrates, our results are likely to be generalisable, and we therefore encourage future studies to further investigate the role of these pathways in shaping dispersal in vertebrates.

The genetic basis of dispersal in a vertebrate metapopulation

“…A recent study on a semi‐natural population of common lizards showed that expression of circadian clock genes differed between dispersers and residents. However, ADORA2A or UPB1 were not among the dispersal‐related genes identified in this species (San‐Jose et al., 2023). Moreover, clock‐linked genes may also influence migratory timing in the American kestrel ( Falco sparverius ; Bossu et al., 2022).…”

Evidence of positive selection and a novel phylogeny among five subspecies of song sparrow (Melospiza melodia) in Alaska

“…Of the 26 candidate genes tested for signals of positive selection, two showed significance: BCO1 (p = 0.037) and KCTD21 (p = 0.032; Table 2). These genes are associated with plumage color and dispersal, respectively (Ruegg et al, 2014; Toews, Hofmeister & Taylor, 2017; San-Jose et al, 2023).…”

“…Potassium channel tetramerization domain, KCTD21 , is associated with dispersal, migration, and the circadian clock (San-Jose et al, 2023). Dispersal and migration are two separate, but possibly intertwined, processes.…”

“…Candidate genes were chosen through a review of literature that identified genes that showed correlations with phenotypes of interest. We chose 34 candidate genes associated with body size (Liu et al, 2015), bill size and shape (Lamichhaney et al, 2015; Chaves et al, 2016; Huang et al, 2022), migration (Vallone et al, 2007; Ruegg et al, 2014; Delmore et al, 2015), dispersal (San-Jose et al, 2023), plumage coloration (Walsh et al, 2011), and salt tolerance (Walsh et al, 2019). Sequences for each gene were obtained from NCBI GenBank (Table S3).…”

Single nucleotide polymorphism SNP19140160 A>C is a potential breeding locus for fast-growth largemouth bass (Micropterus salmoides)

“…The relative lag in genomic research on aquatic species, coupled with the heterogeneity and high complexity of their genomes, has limited the application of high-throughput sequencing techniques. However, recent advancements in RAD-seq have introduced novel tools for studying aquatic species [20][21][22]. This technology has gained widespread popularity in breeding programs because of its many advantages, such as consistent size of digested DNA fragments, streamlined library construction procedures, and high accuracy.…”