A key evolution in gene expression plasticity for freshwater colonisation in early life stage of fish

Abstract

Colonisation of freshwater habitats by marine animals is a remarkable evolutionary event that has enriched biodiversity in freshwater ecosystems. For successful freshwater colonisation, high physiological plasticity is presumed to be necessary, but its evolutionary basis has not been detailed. Marine-originated amphidromous species, which regularly migrate between freshwater and marine environments, have repeatedly lost migratory behaviour in many lineages, which sometimes triggered species radiation in freshwater habitats. Since amphidromous species typically visit the sea during the larval period, the difficulty in the evolution of larval freshwater tolerance is a bottleneck for freshwater colonisation. To elucidate the key evolutionary changes that enhance the physiological plasticity for freshwater colonisation, we compared larval gene expression changes depending on salinity conditions among three congeneric amphidromous goby species (Gymnogobius) with varying dependences on freshwater habitats. First, an otolith microchemical analysis and rearing experiment under laboratory conditions confirmed the presence of freshwater residents only in G. urotaenia and higher larval survivorship of this species both in seawater and freshwater conditions than the obligate amphidromous G. petschiliensis and G. opperiens. Larval whole-body transcriptome analysis revealed that G. urotaenia exhibited the greatest differences in the expression levels of several osmoregulatory genes, including aqp3, which is critical for water discharge from their body during early fish development. Thus, we obtained the results that consistently support the importance of enhanced osmoregulatory plasticity for establishing freshwater forms, and further identified some important evolutionary changes for larval freshwater adaptation and colonisation in the goby group.

Does larval ability to modulate body buoyancy explain successful colonization of freshwater environments by diadromous gobies?

“…Among the three amphidromous species, only G. urotaenia contains several FWR populations in lakes and streams, whereas the others spend their larval periods in the sea (Umino et al, 2015;Oto et al, 2022). A previous study demonstrated the relative superiority of the osmoregulatory performance of G. urotaenia larvae under freshwater conditions (Oto et al, 2022). However, this may not be sufficient to fully explain the life-history variations among Gymnogobius species because of some osmoregulatory flexibility also in the other two species.…”

“…All three species usually spawn in freshwater stream areas, migrate downstream to the sea immediately after birth, drift along the coast for 2-3 months during the larval stage, and return to streams when juveniles, forming large schools (Dotu, 1955;Harada, 2002). However, only G. urotaenia has established freshwater resident (FWR) populations in lakes and streams in several regions (Umino et al, 2015;Oto et al, 2022). No FWR populations have been reported for G. petschiliensis or G. opperiens.…”

“…These samples were common to those used in our previous study (Oto et al, 2022). The UA and UB of G. urotaenia were determined to be the FWR populations by otolith microchemical analysis of the parental males of the egg clutches used in this study (Oto et al, 2022). The water temperature and salinity at each site were recorded using an electronic salinometer Horiba,Ltd.,Kyoto,Japan).…”

“…Among the three amphidromous species, only G. urotaenia contains several FWR populations in lakes and streams, whereas the others spend their larval periods in the sea (Umino et al, 2015;Oto et al, 2022). A previous study demonstrated the relative superiority of the osmoregulatory performance of G. urotaenia larvae under freshwater conditions (Oto et al, 2022).…”

“…Among the several types of diadromy, amphidromy is the most speciose and provides the clearest example in which larval physiology limits the establishment of FWR populations because most amphidromous species enter the sea only in the larval stage, when physiological flexibility is generally low (McDowall, 2007;Augspurger et al, 2017;Delgado and Ruzzante, 2020). Among amphidromous fishes, the FWR form has been observed only in a limited number of species or groups (Tsunagawa and Arai, 2008;Augspurger et al, 2017;Oto et al, 2022). However, no study has yet determined the larval fish characteristics that are critical for the occurrence of FWR populations in amphidromous species.…”