Genomic basis of the loss of diadromy in Galaxias maculatus: Insights from reciprocal transplant experiments

Abstract

Diadromy is known for having major effects on the distribution and richness of aquatic species, and so does its loss. The loss of diadromy has led to the diversification of many species, yet research focusing on understanding its molecular basis and consequences are limited. This is particularly true for amphidromous species despite being the most abundant group of diadromous species. Galaxias maculatus, an amphidromous species and one of the most widely distributed fishes in the Southern Hemisphere, exhibits many instances of nonmigratory or resident populations. The existence of naturally replicated resident populations in Patagonia can serve as an ideal system for the study of the mechanisms that lead to the loss of the diadromy and its ecological and evolutionary consequences. Here, we studied two adjacent river systems in which resident populations are genetically differentiated yet derived from the same diadromous population. By combining a reciprocal transplant experiment with genomic data, we showed that the two resident populations followed different evolutionary pathways by exhibiting a differential response in their capacity to survive in salt water. While one resident population was able to survive salt water, the other was not. Genomic analyses provided insights into the genes that distinguished (a) migratory from nonmigratory populations; (b) populations that can vs those that cannot survive a saltwater environment; and (c) between these resident populations. This study demonstrates that the loss of diadromy can be achieved by different pathways and that environmental (selection) and random (genetic drift) forces shape this dynamic evolutionary process.

Does assortative mating contribute to reproductive isolation among sympatric ecotypes of the wing‐dimorphic stonefly Zelandoperla fenestrata (Plecoptera: Gripopterygidae)?

“…2020) and for understanding the basis of reproductive isolation among recently diverged lineages (Delgado et al . 2020).…”

Investigating Diadromy in Fishes and Its Loss in an -Omics Era

“…(2019) Populations diversity and structure Galaxias maculatus Yes Delgado et al. (2019) Salinity adaptation Galaxias maculatus Yes Delgado et al. (2020) Transcriptomics (transcriptome sequencing) Salinity adaptation Plecoglossus altivelis Yes Lu et al.…”

“…Reciprocal transplant experiments with common galaxias under laboratory conditions also revealed that resident populations can differ in their response to salinity changes with some populations maintaining their osmoregulatory performance necessary for migration and others not being able to survive such changes ( Delgado et al., 2020 ). Given that these populations were similarly genetically differentiated from their diadromous counterpart, we suspect genetic drift may be one of the factors playing an important role in determining whether the ability to migrate is maintained or lost.…”

“…Research in salmonids has shown little parallelism in genes differentiating diadromous and resident populations across species ( Schneider et al., 2019 ). Even within the same species, replicate resident populations show that local adaptation and genetic drift can lead to different genes being fixed or lost ( Delgado et al., 2020 ; Salisbury et al., 2020 ). Thus, further research on a variety of species and tissues including brain is necessary to improve our understanding of the genes that may be common among diadromous species.…”

Unpacking the complexity of longitudinal movement and recruitment patterns of facultative amphidromous fish

“…Amphidromy is the most frequent among diadromous migratory strategies 11 and was classically described as spawning in freshwater riverine habitats with subsequent larvae transport downstream and development in marine habitats, and juvenile migration back to freshwater habitats to complete growth to adults 12 . However, recent studies have shown that some populations of amphidromous species may lose migratory traits and develop resident populations 13,14 . These facultative amphidromous fish species are characterised by a complex pattern of migratory and resident…”