Transcriptomic differentiation underlying marine‐to‐freshwater transitions in the South American silversides Odontesthes argentinensis and O. bonariensis (Atheriniformes)

Abstract

Salinity gradients are critical habitat determinants for freshwater organisms. Silverside fishes in the genus Odontesthes have recently and repeatedly transitioned from marine to freshwater habitats, overcoming a strong ecological barrier. Genomic and transcriptomic changes involved in this kind of transition are only known for a few model species. We present new data and analyses of gene expression and microbiome composition in the gills of two closely related silverside species, marine O. argentinensis and freshwater O. bonariensis and find more than three thousand transcripts differentially expressed, with osmoregulatory/ion transport genes and immune genes showing very different expression patterns across species. Interspecific differences also involve more than one thousand transcripts with nonsynonymous SNPs in the coding sequences, most of which were not differentially expressed. In addition to characterizing gill transcriptomes from wild-caught marine and freshwater fishes, we test experimentally the response to salinity increases by O. bonariensis collected from freshwater habitats. Patterns of expression in gill transcriptomes of O. bonariensis exposed to high salinity do not resemble O. argentinensis mRNA expression, suggesting lack of plasticity for adaptation to marine conditions in this species. The diversity of functions associated with both the differentially expressed set of transcripts and those with sequence divergence plus marked microbiome differences suggest that multiple abiotic and biotic factors in marine and freshwater habitats are driving transcriptomic differences between these species. K E Y W O R D S

Evaluation of Reference Genes to Analyze Gene Expression in Silverside Odontesthes humensis Under Different Environmental Conditions

“…In these regions, some species have economic importance for production, flesh commercialization and sport fishing (Menone et al, 2000 ; Somoza et al, 2008 ). Furthermore, some silversides have been used as experimental models for evolutionary, osmoregulatory, and environmental pollution studies due to the radiation after continental waters invasion from ocean, euryhaline biology and inhabitation of environments contaminated by glyphosate coming from rice and soybean monocultures in fields near to the habitat of silversides (Menone et al, 2000 ; Carriquiriborde and Ronco, 2006 ; Tsuzuki et al, 2007 ; Piedras et al, 2009 ; Bloom et al, 2013 ; Hughes et al, 2017 ; Zebral et al, 2017 ). Moreover, the silversides have already been utilized to address various aspects of gene expression (Strobl-Mazzulla et al, 2005 ; Karube et al, 2007 ; Fernandino et al, 2008 , 2011 ; Majhi et al, 2009 ; Miranda et al, 2009 ; Blasco et al, 2010 ; Gómez-Requeni et al, 2012 ; Pérez et al, 2012 ; González et al, 2015 ).…”

Biogeography, habitat transitions and hybridization in a radiation of South American silverside fishes revealed by mitochondrial and genomic RAD data

“…A recent study comparing gene expression profiles in gills of wild‐caught O. bonariensis (freshwater) and O. argentinensis (marine) revealed significant differences between these two species for more than 3,000 transcripts, some of them coding for osmoregulatory/ion transport and immune system functions (Hughes et al, ). Additionally, more than 1,000 transcripts with nonsynonymous SNPs in the coding sequences were found to be different between the species.…”

“…New World silversides (family Atherinopsidae) have repeatedly transitioned between marine and freshwater habitats, but precise knowledge of their phylogenetic history, and therefore the chronology and frequency of inferred habitat transitions, remains contentious (Bloom, Weir, Piller, & Lovejoy, ; Campanella et al, ; Dyer, ). Some freshwater silverside species can osmoregulate in brackish water (Hughes, Somoza, & Nguyen, ; Silveira, Martins, & Domingues, ; Tsuzuki, Aikawá, Strüssmann, & Takashima, ), suggesting that reversals from freshwater to marine habitats may be possible, despite this being a relatively rare phenomenon among ray‐finned fishes (Betancur‐R, Ortí, & Pyron, ). With seven marine and 12 freshwater recognized species (Fricke, Eschmeyer, & van der Laan, ) distributed across coastal marine habitats and in rivers and lakes exclusively in temperate South America (Figure a,b), the atherinopsid genus Odontesthes (locally known as pejerrey in Spanish or peixe‐rei in Portuguese) provides a unique system to study the history and evolutionary consequences of habitat transitions.…”

“…New World silversides (family Atherinopsidae) have repeatedly transitioned between marine and freshwater habitats, but precise knowledge of their phylogenetic history, and therefore the chronology and frequency of inferred habitat transitions, remains contentious (Bloom, Weir, Piller, & Lovejoy, 2013;Campanella et al, 2015;Dyer, 2006). Some freshwater silverside species can osmoregulate in brackish water (Hughes, Somoza, & Nguyen, 2017;Silveira, Martins, & Domingues, 2018;Tsuzuki, Aikawá, Strüssmann, & Takashima, 2000), suggesting that reversals from freshwater to marine habitats may be possible, despite this being a relatively rare phenomenon among ray-finned fishes (Betancur-R, Ortí, & Pyron, 2015).…”

Genome-wide selection scans integrated with association mapping reveal mechanisms of physiological adaptation across a salinity gradient in killifish

“…Tight junctions form at intercellular junctions and work to regulate the flow of solutes through the paracellular pathway [79]. Tight junction proteins are well-known components of the osmoregulatory apparatus in fish [71], and have been identified as regulators of variation in osmotic tolerance in stickleback [31], killifish [80], alewives [81], silverside [82], and sea bass [83], among others. At low salinity, tight junctions prevent the loss of Clwhile leaky junctions at high salinity enable the excretion of Na.…”