Landlocking of diadromous fish in freshwater systems can have significant genomic consequences. For instance, the loss of the migratory life stage can dramatically reduce gene flow across populations, leading to increased genetic structuring, and stronger effects of local adaptation. These genomic consequences have been well-studied in some mainland systems, but the evolutionary impacts of landlocking in island ecosystems are largely unknown. In this study, we used a genotyping-by-sequencing (GBS) approach to examine the evolutionary history of landlocking in common smelt (Retropinna retropinna) on Chatham Island, a small isolated oceanic island 650 km southeast of mainland New Zealand. We examined the relationship among the Chatham Island and mainland smelt, and used coalescent analyses to test the number and timing of landlocking events on Chatham Island. Our genomic analysis, based on 21,135 SNPs across 169 individuals, revealed that the Chatham Island smelt were genomically distinct from the mainland New Zealand fish, consistent with a single ancestral colonisation event of Chatham Island in the Pleistocene. Significant genetic structure was also evident within the Chatham Island smelt, with a diadromous Chatham Island smelt group, along with three geographically structured landlocked groups. Coalescent demographic analysis supported three independent landlocking events, with this loss of diadromy significantly pre-dating human colonisation. Our results illustrate how landlocking of diadromous fish can occur repeatedly across a narrow spatial scale, and highlight a unique system to study the genomic basis of repeated adaptation.

Landlocking is a process whereby a population of normally diadromous fish becomes limited to freshwater, potentially leading to behavioural, morphological, and genetic changes, and occasionally speciation. The study of recently landlocked populations can shed light on how populations adapt to environmental change, and how such life-history shifts affect population-genetic structure. Kōaro (Galaxias brevipinnis) is a facultatively diadromous Southern Hemisphere galaxiid fish that frequently becomes landlocked in inland lakes. This study compares seven landlocked kōaro populations to diadromous populations from main and offshore islands of New Zealand. Genotyping-by-sequencing was used to obtain genotypes at 18,813 single nucleotide polymorphism sites for each population. Analyses of population structure revealed that most landlocked populations were genetically highly distinct from one another, as well as from diadromous populations. A few particularly isolated island and lake populations were particularly strongly genetically differentiated. Landscape characteristics were measured to test whether lake elevation, size, or distance from the sea predicted genetic diversity or differentiation from diadromous kōaro. While there were no significant relationships indicating isolation-by-distance or isolation-by-environment, we detected a trend toward lower genetic diversity in lakes at higher elevations. Our findings illustrate the critical role that landlocking can play in the structure of intraspecific genetic diversity within and between populations.

Processes responsible for population structuring across spatial and temporal scales represent key components in understanding speciation and evolution. We use a hierarchical approach to investigate the degree and mechanisms of structuring in landlocked and diadromous populations of the facultatively amphidromous fish Galaxias brevipinnis across various temporal and spatial scales in southern New Zealand. To determine long-term structuring, multiple lakes and coastal sites were compared genetically. Short-term structuring was assessed using otolith microchemistry for a subset of sites, and behavioural mechanisms driving population structuring were assessed via larval distributions. Genetic data show that lakes foster divergence of lake-developing populations from each other and from coastal stream populations, whereas there is relatively little structuring within coast or lake populations. However, otolith analyses indicate that on a shorter time scale, most larvae do not disperse, i.e. recruitment is local. Thus, lake and coastal populations show a distinct meta-population structure based on catchment, in contrast to the prevailing assumption of widespread dispersal, with implications for management. Most larvae were distributed in river plumes, suggesting that a simple larval behavioural mechanism, e.g. positive rheotaxis, may result in larval retention within catchments and lakes. However, not all larvae were retained in plumes, creating opportunities for genetic exchange within-lake or among coastal sites. Genetic divergence of lake populations as a consequence of landscape and behaviour provides an insight into the potential of G. brevipinnis to diversify and speciate, when landscape and circumstances align, and also has implications for the management of this and other facultatively amphidromous species.