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Evolution and molecular mechanisms of adaptive organ allometry in Atlantic salmon (Salmo salar)

Periodic Reporting for period 1 - SalmoScales (Evolution and molecular mechanisms of adaptive organ allometry in Atlantic salmon (Salmo salar))

Reporting period: 2023-09-01 to 2025-08-31

Differences in body proportions for a similar body plan are responsible for much of species diversity, famously referred to as "endless forms most beautiful" by Darwin. Within a particular species, however, the proportions of body parts and organs typically remain constant. This guarantees a functional body; variation in organ proportions can be signs of developmental conditions or disease such as cancer. To better understand the cellular and genetic processes giving rise to differences in proportions (termed allometry), the SalmoScales project studied a case of allometry in ovary size following freshwater adaptation in Atlantic salmon. Landlocked salmon on the island of Newfoundland, Canada, have adapted to resource-limited streams by evolving into dwarfs; they become sexually mature at extremely young age for a salmon, and as small as 10cm in length. Dwarfism in salmon is accompanied by atypical ovarian development where the ovaries of dwarfs are half the size of anadromous salmon, providing for a unique natural system where the mechanisms encoding for allometry can be studied in the context of alternative life-histories. By using latest genomics technologies, the aim in this project is to yield novel insight into the molecular machinery that establishes differences in organ proportions and how conserved they are between species. The results can guide, for example, novel breeding methods in aquaculture and inform medical research about the mechanisms that coordinate growth and differentiation.
In collaboration with researchers at Concordia University, Montreal, we designed a common-garden experiment where the developmental and genetic differences between dwarf and anadromous Atlantic salmon can be studied in controlled environmental conditions. Through fieldwork during the breeding season of the dwarf salmon we gained new insight into their previously unknown reproductive ecology and behavior. Contrary to previous research that indicated a maximum fecundity of ~30 eggs per dwarf salmon female, our field-observations indicate that the number of ripe eggs may vary between 1-28 depending on the female. This suggests that the dwarf salmon females may lay as few as a single egg at a time when spawning. Because breeding may happen with different males each time, these observations indicate that dwarf salmon populations may harbor more genetic diversity that would be expected given their extremely small population sizes. Furthermore, we field-collected gametes from dwarf salmon from two small streams in Cape Race, Newfoundland, using electrofishing and transported the gametes to Concordia University Aquatic Facilities. In addition, we collected gametes from anadromous Atlantic salmon that were captured from the Saint-Mary’s River in Nova Scotia, Canada, and raised at a Canadian governmental hatchery. The gametes were used to establish populations of dwarf and anadromous Atlantic salmon, and their F1 hybrids, at common environmental conditions at Concordia University. These populations, which have been established following a breeding design allowing the study of their genetic characteristics, allows for unique experimental procedures to be performed that will reveal the molecular mechanisms of allometry in salmon reproductive development. We further established cell cultures of a gonad cell line from rainbow trout that will allow for the in vivo validation of the function of the genetic mechanisms discovered in controlling cellular development such as cell size and proliferation.
The SalmoScales project provides a first proof-of-concept that dwarf Atlantic salmon can be bred in controlled conditions and used as a model species for studying the evolution allometry differences within species. The captive populations of dwarf, anadromous and dwarf-anadromous hybrid salmon established in the project, being world’s first of their kind, serve as a unique platform for further research in not only the mechanisms and genetic basis of allometry, but also to discover the genetic basis of their other characteristics such as extremely young age at maturity and distinctive morphology. They can further be used to study freshwater adaptation such as immunity traits and growth characteristics that may be of value for developing salmon aquaculture strains that perform well in captive freshwater conditions such as used in environmentally friendly land-based aquaculture. Further research should capitalize on the established populations to elucidate on the genetic characteristics and molecular mechanisms encoding for the unique life-history and reproductive development of the dwarf Atlantic salmon.
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