BACKGROUND: Smell abilities differ greatly among vertebrate species due to distinct sensory needs, with exceptional variability reported in the number of olfactory genes and the size of the odour-processing regions of the brain. However, key environmental factors shaping genomic and phenotypic changes linked to the olfactory system remain difficult to identify at macroevolutionary scales. Here, we investigate the association between diverse ecological traits and the number of olfactory chemoreceptors in approximately two hundred ray-finned fishes. RESULTS: We found independent expansions producing large gene repertoires in several lineages of nocturnal amphibious fishes, generally able to perform active terrestrial exploration. We reinforced this finding with on-purpose genomic and transcriptomic analysis of Channallabes apus, a catfish species from a clade with chemosensory-based aerial orientation. Furthermore, we also detected an augmented information-processing capacity in the olfactory bulb of nocturnal amphibious fishes by estimating the number of cells contained in this brain region in twenty-four actinopterygian species. CONCLUSIONS: Overall, we report a convergent genomic and phenotypic magnification of the olfactory system in nocturnal amphibious fishes. This finding suggests the possibility of an analogous evolutionary event in fish-like tetrapod ancestors during the first steps of the water-to-land transition, favouring terrestrial adaptation through enhanced aerial orientation.

Biozentrum University of Basel Basel Switzerland

Department of Zoology Faculty of Science Charles University Prague Czech Republic

Max Planck Institute of Molecular Cell Biology and Genetics Dresden Germany

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Imai T, Sakano H. Odorant receptor gene choice and axonal projection in the mouse olfactory system. Results Probl Cell Differ. 2009 doi: 10.1007/400_2008_3. PubMed DOI

Saraiva LR, Ahuja G, Ivandic I, Syed AS, Marioni JC, Korsching SI, et al. Molecular and neuronal homology between the olfactory systems of zebrafish and mouse. Sci Rep. 2015;5:11487. doi: 10.1038/srep11487. PubMed DOI PMC

Dang P, Fisher SA, Stefanik D, Kim J, Raper JA. Coordination of olfactory receptor choice with guidance receptor expression and function in olfactory sensory neurons. PLoS Genet. 2018 doi: 10.1371/journal.pgen.1007164. PubMed DOI PMC

Iwaniuk AN. 1.18 - Functional Correlates of Brain and Brain Region Sizes in Nonmammalian Vertebrates. In: Kaas JHBT-E of NS, editor. 2nd ed. Oxford: Academic Press; 2017. p. 335–48.

Zelenitsky DK, Therrien F, Ridgely RC, McGee AR, Witmer LM. Evolution of olfaction in non-avian theropod dinosaurs and birds. Proc R Soc B Biol Sci. 2011;278:3625–3634. doi: 10.1098/rspb.2011.0238. PubMed DOI PMC

Wagner H. Sensory Brain Areas in Mesopelagic Fishes. Brain Behav Evol. 2001;57:117–133. doi: 10.1159/000047231. PubMed DOI

Poncelet G, Shimeld SM. The evolutionary origins of the vertebrate olfactory system. Open Biol. 2022;10:200330. doi: 10.1098/rsob.200330. PubMed DOI PMC

Niimura Y. On the origin and evolution of vertebrate olfactory receptor genes: comparative genome analysis among 23 chordate species. Genome Biol Evol. 2009;1:34–44. doi: 10.1093/gbe/evp003. PubMed DOI PMC

Silva L, Antunes A. Vomeronasal receptors in vertebrates and the evolution of pheromone detection. Annu Rev Anim Biosci. 2017;5:353–370. doi: 10.1146/annurev-animal-022516-022801. PubMed DOI

Eyun S-I, Moriyama H, Hoffmann FG, Moriyama EN. Molecular evolution and functional divergence of trace amine-associated receptors. PLoS One. 2016;11:e0151023. doi: 10.1371/journal.pone.0151023. PubMed DOI PMC

Niimura Y. Olfactory receptor multigene family in vertebrates: from the viewpoint of evolutionary genomics. Curr Genomics. 2012;13:103–114. doi: 10.2174/138920212799860706. PubMed DOI PMC

Lin Q, Fan S, Zhang Y, Xu M, Zhang H, Yang Y, et al. The seahorse genome and the evolution of its specialized morphology. Nature. 2016;540:395–399. doi: 10.1038/nature20595. PubMed DOI PMC

Policarpo M, Bemis KE, Tyler JC, Metcalfe CJ, Laurenti P, Sandoz JC, et al. Evolutionary Dynamics of the OR Gene Repertoire in Teleost Fishes: Evidence of an Association with Changes in Olfactory Epithelium Shape. Mol Biol Evol. 2021;38:3742–3753. doi: 10.1093/molbev/msab145. PubMed DOI PMC

Policarpo M, Bemis KE, Laurenti P, Legendre L, Sandoz JC, Rétaux S, et al. Coevolution of the olfactory organ and its receptor repertoire in ray-finned fishes. BMC Biol. 2022;20:195. doi: 10.1186/s12915-022-01397-x. PubMed DOI PMC

Liu H, Chen C, Lv M, Liu N, Hu Y, Zhang H, et al. A chromosome-level assembly of blunt snout bream (Megalobrama amblycephala) genome reveals an expansion of olfactory receptor genes in freshwater fish. Mol Biol Evol. 2021;38:4238–4251. doi: 10.1093/molbev/msab152. PubMed DOI PMC

Niimura Y, Matsui A, Touhara K. Extreme expansion of the olfactory receptor gene repertoire in African elephants and evolutionary dynamics of orthologous gene groups in 13 placental mammals. Genome Res. 2014;24:1485–1496. doi: 10.1101/gr.169532.113. PubMed DOI PMC

Oka Y, Saraiva LR, Korsching SI. Crypt neurons express a single V1R-related ora gene. Chem Senses. 2012;37:219–227. doi: 10.1093/chemse/bjr095. PubMed DOI

Olivares J, Schmachtenberg O. An update on anatomy and function of the teleost olfactory system. PeerJ. 2019;7:e7808. doi: 10.7717/peerj.7808. PubMed DOI PMC

Wright PA, Turko AJ. Amphibious fishes: evolution and phenotypic plasticity. J Exp Biol. 2016;219(Pt 15):2245–2259. doi: 10.1242/jeb.126649. PubMed DOI

Ord TJ, Cooke GM. Repeated evolution of amphibious behavior in fish and its implications for the colonization of novel environments. Evolution (N Y) 2016;70:1747–1759. PubMed

Sayer MDJ, Davenport J. Amphibious fish: why do they leave water? Rev Fish Biol Fish. 1991;1:159–181. doi: 10.1007/BF00157583. DOI

Bressman NR, Farina SC, Gibb AC. Look before you leap: Visual navigation and terrestrial locomotion of the intertidal killifish Fundulus heteroclitus. J Exp Zool Part A Ecol Genet Physiol. 2016;325:57–64. doi: 10.1002/jez.1996. PubMed DOI

Bressman NR, Simms M, Perlman BM, Ashley-Ross MA. Where do fish go when stranded on land? Terrestrial orientation of the mangrove rivulus Kryptolebias marmoratus. J Fish Biol. 2019;95:335–344. doi: 10.1111/jfb.13802. PubMed DOI

Bressman NR, Hill JE, Ashley-Ross MA. Why did the invasive walking catfish cross the road? Terrestrial chemoreception described for the first time in a fish. J Fish Biol. 2020;97:895–907. doi: 10.1111/jfb.14465. PubMed DOI

Van Wassenbergh S, Herrel A, Adriaens D, Huysentruyt F, Devaere S, Aerts P. Evolution: a catfish that can strike its prey on land. Nature. 2006;440:881. doi: 10.1038/440881a. PubMed DOI

Van Wassenbergh S. Kinematics of terrestrial capture of prey by the eel-catfish Channallabes apus. Integr Comp Biol. 2013;53:258–268. doi: 10.1093/icb/ict036. PubMed DOI

Kotrschal K, Van Staaden MJ, Huber R. Fish Brains: Evolution and Anvironmental Relationships. Rev Fish Biol Fish. 1998;8:373–408. doi: 10.1023/A:1008839605380. DOI

Kverková K, Marhounová L, Polonyiová A, Kocourek M, Zhang Y, Olkowicz S, et al. The evolution of brain neuron numbers in amniotes. Proc Natl Acad Sci. 2022;119:e2121624119. doi: 10.1073/pnas.2121624119. PubMed DOI PMC

Braubach OR, Fine A, Croll RP. Distribution and functional organization of glomeruli in the olfactory bulbs of zebrafish (Danio rerio) J Comp Neurol. 2012;520:2317–2339. doi: 10.1002/cne.23075. PubMed DOI

Weiss L, Manzini I, Hassenklöver T. Olfaction across the water–air interface in anuran amphibians. Cell Tissue Res. 2021;383:301–325. doi: 10.1007/s00441-020-03377-5. PubMed DOI PMC

Kishida T. Olfaction of aquatic amniotes. Cell Tissue Res. 2021;383:353–365. doi: 10.1007/s00441-020-03382-8. PubMed DOI

Tatsumi N, Kobayashi R, Yano T, Noda M, Fujimura K, Okada N, et al. Molecular developmental mechanism in polypterid fish provides insight into the origin of vertebrate lungs. Sci Rep. 2016;6:30580. doi: 10.1038/srep30580. PubMed DOI PMC

Amemiya CT, Alföldi J, Lee AP, Fan S, Philippe H, MacCallum I, et al. The African coelacanth genome provides insights into tetrapod evolution. Nature. 2013;496:311–316. doi: 10.1038/nature12027. PubMed DOI PMC

Mollo E, Fontana A, Roussis V, Polese G, Amodeo P, Ghiselin MT. Sensing marine biomolecules: smell, taste, and the evolutionary transition from aquatic to terrestrial life. Front Chem. 2014;2:92. doi: 10.3389/fchem.2014.00092. PubMed DOI PMC

Nevitt GA, Dittman AH, Quinn TP, Moody WJJ. Evidence for a peripheral olfactory memory in imprinted salmon. Proc Natl Acad Sci U S A. 1994;91:4288–4292. doi: 10.1073/pnas.91.10.4288. PubMed DOI PMC

Li Q. Deorphanization of olfactory trace amine-associated receptors. Methods Mol Biol. 2018;1820:21–31. doi: 10.1007/978-1-4939-8609-5_2. PubMed DOI

Boschat C, Pélofi C, Randin O, Roppolo D, Lüscher C, Broillet M-C, et al. Pheromone detection mediated by a V1r vomeronasal receptor. Nat Neurosci. 2002;5:1261–1262. doi: 10.1038/nn978. PubMed DOI

Cichy A, Shah A, Dewan A, Kaye S, Bozza T. Genetic depletion of class I odorant receptors impacts perception of carboxylic acids. Curr Biol. 2019;29:2687–2697.e4. doi: 10.1016/j.cub.2019.06.085. PubMed DOI PMC

Meyer A, Schloissnig S, Franchini P, Du K, Woltering JM, Irisarri I, et al. Giant lungfish genome elucidates the conquest of land by vertebrates. Nature. 2021;590:284–289. doi: 10.1038/s41586-021-03198-8. PubMed DOI PMC

Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34:i884–i890. doi: 10.1093/bioinformatics/bty560. PubMed DOI PMC

Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods. 2017;14:417–419. doi: 10.1038/nmeth.4197. PubMed DOI PMC

Ibarra-Soria X, Nakahara TS, Lilue J, Jiang Y, Trimmer C, Souza MAA, et al. Variation in olfactory neuron repertoires is genetically controlled and environmentally modulated. Elife. 2017;6:e21476. doi: 10.7554/eLife.21476. PubMed DOI PMC

Zhang Z, Sakuma A, Kuraku S, Nikaido M. Remarkable diversity of vomeronasal type 2 receptor (OlfC) genes of basal ray-finned fish and its evolutionary trajectory in jawed vertebrates. Sci Rep. 2022;12:6455. doi: 10.1038/s41598-022-10428-0. PubMed DOI PMC

Matschiner M, Böhne A, Ronco F, Salzburger W. The genomic timeline of cichlid fish diversification across continents. Nat Commun. 2020;11:5895. doi: 10.1038/s41467-020-17827-9. PubMed DOI PMC

Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol Biol Evol. 2013;30:772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC

Betancur-R R, Broughton RE, Wiley EO, Carpenter K, López JA, Li C, et al. The tree of life and a new classification of bony fishes. PLoS Curr tree life. 2013;5. PubMed PMC

Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020;37:1530–1534. doi: 10.1093/molbev/msaa015. PubMed DOI PMC

Bürkner PC. brms: an R package for Bayesian multilevel models using stan. J Stat Softw. 2017;80 1 SE-Articles:1–28.

Baid G, Cook DE, Shafin K, Yun T, Llinares-López F, Berthet Q, et al. DeepConsensus: gap-aware sequence transformers for sequence correction. bioRxiv. 2021:2021.08.31.458403.

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI

Cheng H, Concepcion GT, Feng X, Zhang H, Li H. Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. Nat Methods. 2021;18:170–175. doi: 10.1038/s41592-020-01056-5. PubMed DOI PMC

Guan D, McCarthy SA, Wood J, Howe K, Wang Y, Durbin R. Identifying and removing haplotypic duplication in primary genome assemblies. Bioinformatics. 2020;36:2896–2898. doi: 10.1093/bioinformatics/btaa025. PubMed DOI PMC

Zhou C, McCarthy SA, Durbin R. YaHS: yet another Hi-C scaffolding tool. bioRxiv. 2022:2022.06.09.495093. PubMed PMC

Poplin R, Chang P-C, Alexander D, Schwartz S, Colthurst T, Ku A, et al. A universal SNP and small-indel variant caller using deep neural networks. Nat Biotechnol. 2018;36:983–987. doi: 10.1038/nbt.4235. PubMed DOI

Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V, Pollard MO, et al. Twelve years of SAMtools and BCFtools. Gigascience. 2021;10:giab008. doi: 10.1093/gigascience/giab008. PubMed DOI PMC

Herculano-Houzel S, Lent R. Isotropic Fractionator: A Simple, Rapid Method for the Quantification of Total Cell and Neuron Numbers in the Brain. J Neurosci. 2005;25:2518 LP–2521. doi: 10.1523/JNEUROSCI.4526-04.2005. PubMed DOI PMC

Pinheiro JC, Bates D, DebRoy S. The R Core Team nlme: Linear and Nonlinear Mixed Effects Models. R Packag nlme version. 2007;3:1–83.