Fish out of water: Genomic insights into persistence of rainbowfish populations in the desert.
Adaptive resilience
arid zone
climate change
freshwater fish
landscape genomics
metapopulation
Journal
Evolution; international journal of organic evolution
ISSN: 1558-5646
Titre abrégé: Evolution
Pays: United States
ID NLM: 0373224
Informations de publication
Date de publication:
01 2022
01 2022
Historique:
revised:
22
10
2021
received:
20
09
2021
accepted:
31
10
2021
pubmed:
16
11
2021
medline:
5
3
2022
entrez:
15
11
2021
Statut:
ppublish
Résumé
How populations of aquatic fauna persist in extreme desert environments is an enigma. Individuals often breed and disperse during favorable conditions. Theory predicts that adaptive capacity should be low in small populations, such as in desert fishes. We integrated satellite-derived surface water data and population genomic diversity from 20,294 single-nucleotide polymorphisms across 344 individuals to understand metapopulation persistence of the desert rainbowfish (Melanotaenia splendida tatei) in central Australia. Desert rainbowfish showed very small effective population sizes, especially at peripheral populations, and low connectivity between river catchments. Yet, there was no evidence of population-level inbreeding and a signal of possible adaptive divergence associated with aridity was detected. Candidate genes for local adaptation included functions related to environmental cues and stressful conditions. Eco-evolutionary modeling showed that positive selection in refugial subpopulations combined with connectivity during flood periods can enable retention of adaptive diversity. Our study suggests that adaptive variation can be maintained in small populations and integrate with neutral metapopulation processes to allow persistence in the desert.
Substances chimiques
Water
059QF0KO0R
Banques de données
figshare
['10.6084/m9.figshare.16915669.v1']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
171-183Informations de copyright
© 2021 The Authors. Evolution © 2021 The Society for the Study of Evolution.
Références
Agnèse, J. -F., H. Louizi, A. Gilles, O. Berrada Rkhami, A. Benhoussa, A. Qninba, and A. Pariselle. 2018. A euryhaline fish, lost in the desert: the unexpected metapopulation structure of Coptodon guineensis (Günther, 1862) in the Sebkha of Imlili. C. R. Biol. 341:75-84.
Alexander, D. H., J. Novembre, and K. Lange. 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19:1655-1664.
AnvariFar, H., A. K. Amirkolaie, H. K. Miandare, H. Ouraji, M. A. Jalali, and S. İ. Üçüncü. 2017. Apoptosis in fish: environmental factors and programmed cell death. Cell Tissue Res. 368:425-439.
Attard, C. R. M., C. J. Brauer, J. Sandoval-Castillo, L. K. Faulks, P. J. Unmack, D. M. Gilligan, and L. B. Beheregaray. 2018. Ecological disturbance influences adaptive divergence despite high gene flow in golden perch (Macquaria ambigua): implications for management and resilience to climate change. Mol. Ecol. 27:196-215.
Barrett, R. D. H. and D. Schluter. 2008. Adaptation from standing genetic variation. Trends Ecol. Evol. 23:38-44.
Bay, R. A., R. J. Harrigan, V. L. Underwood, H. L. Gibbs, T. B. Smith, and K. Ruegg. 2018. Genomic signals of selection predict climate-driven population declines in a migratory bird. Science 359:83-86.
Beheregaray, L. B., L. V. Pfeiffer, C. R. M. Attard, J. Sandoval-Castillo, F. Domingos, L. K. Faulks, D. M. Gilligan, and P. J. Unmack. 2017. Genome-wide data delimits multiple climate-determined species ranges in a widespread Australian fish, the golden perch (Macquaria ambigua). Mol. Phylogen. Evol. 111:65-75.
Bell, G. and A. Gonzalez. 2011. Adaptation and evolutionary rescue in metapopulations experiencing environmental deterioration. Science 332:1327-1330.
Bernardi, G., G. Ruiz-Campos, and F. Camarena-Rosales. 2007. Genetic isolation and evolutionary history of oases populations of the Baja California killifish, Fundulus lima. Conserv. Genet. 8:547-554.
Black, A. N., H. A. Seears, C. M. Hollenbeck, and P. B. Samollow. 2017. Rapid genetic and morphologic divergence between captive and wild populations of the endangered Leon Springs pupfish, Cyprinodon bovinus. Mol. Ecol. 26:2237-2256.
Böhne, A., T. Sengstag, and W. Salzburger. 2014. Comparative transcriptomics in east African cichlids reveals sex- and species-specific expression and new candidates for sex differentiation in fishes. Genome Biol. Evol. 6:2567-2585.
Brauer, C. J., P. J. Unmack, S. Smith, L. Bernatchez, and L. B. Beheregaray. 2018. On the roles of landscape heterogeneity and environmental variation in determining population genomic structure in a dendritic system. Mol. Ecol. 27:3484-3497.
Carini, G. and J. M. Hughes. 2006. Subdivided population structure and phylogeography of an endangered freshwater snail, Notopala sublineata (Conrad, 1850) (Gastropoda: Viviparidae), in Western Queensland, Australia. Biol. J. Linn. Soc. 88:1-16.
Chafin, T. K., M. R. Douglas, B. T. Martin, and M. E. Douglas. 2019. Hybridization drives genetic erosion in sympatric desert fishes of western North America. Heredity 123:759-773.
Chen, Z., A. P. Farrell, A. Matala, N. Hoffman, and S. R. Narum. 2018a. Physiological and genomic signatures of evolutionary thermal adaptation in redband trout from extreme climates. Evol. Appl. 11:1686-1699.
Chen, Z., Farrell, A. P., Matala, Z., and Narum, S. R. 2018b. Mechanisms of thermal adaptation and evolutionary potential of conspecific populations to changing environments. Mol. Ecol. 27 659-674. https://doi.org/10.1111/mec.14475.
Chitnis, A. B., D. Dalle Nogare, and M. Matsuda. 2012. Building the posterior lateral line system in zebrafish. Dev. Neurobiol. 72:234-255.
Costelloe, J. F., R. B. Grayson, T. A. McMahon, and R. M. Argent. 2005. Spatial and temporal variability of water salinity in an ephemeral, arid-zone river, central Australia. Hydrol. Process. 19:3147-3166.
Costelloe, J. F. and K. L. Russell. 2014. Identifying conservation priorities for aquatic refugia in an arid zone, ephemeral catchment: a hydrological approach. Ecohydrology 7:1534-1544.
de Villemereuil, P. and O. E. Gaggiotti. 2015. A new FST-based method to uncover local adaptation using environmental variables. Methods Ecol. Evol. 6:1248-1258. https://doi.org/10.1111/2041-210X.12418.
DeVogel, S. B., J. W. Magee, W. F. Manley, and G. H. Miller. 2004. A GIS-based reconstruction of late Quaternary paleohydrology: Lake Eyre, arid central Australia. Palaeogeogr. Palaeoclimatol. Palaeoecol. 204: 1-13.
Do, C., R. S. Waples, D. Peel, G. M. Macbeth, B. J. Tillett, and J. R. Ovenden. 2014. NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol. Ecol. Resour. 14:209-214.
Excoffier, L. and H. E. L. Lischer. 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10:564-567.
Foll, M. and O. Gaggiotti. 2008. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977-993.
Frankham, R., J. D. Ballou, and D. A. Briscoe. 2002. Introduction to conservation genetics. Cambridge Univ. Press, Cambridge, U.K.
Frankham, R., C. J. A. Bradshaw, and B. W. Brook. 2014. Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biol. Conserv. 170:56-63.
Fraser, D. J. 2017. Genetic diversity of small populations: not always “doom and gloom”? Mol. Ecol. 26:6499-6501.
Gao, S., S. Liu, J. Yao, T. Zhou, N. Li, Q. Li, R. Dunham, Z. Liu. 2017. Taste receptors and gustatory associated G proteins in channel catfish, Ictalurus punctatus. Comp. Biochem. Physiol. D Genom. Proteom. 21:1-9.
Gates, K., J. Sandoval-Castillo, L. Bernatchez, and L. B. Beheregaray. 2017. De novo transcriptome assembly and annotation for the desert rainbowfish (Melanotaenia splendida tatei) with comparison with candidate genes for future climates. Mar. Genomics 35:63-68.
Gouin, N., A. Bertin, M. I. Espinosa, D. D. Snow, J. M. Ali, and A. S. Kolok. 2019. Pesticide contamination drives adaptive genetic variation in the endemic mayfly Andesiops torrens within a semi-arid agricultural watershed of Chile. Environ. Pollut. 255:113099.
Gross, J. B., A. Furterer, B. M. Carlson, and B. A. Stahl. 2013. An integrated transcriptome-wide analysis of cave and surface dwelling Astyanax mexicanus. PLoS ONE 8:e55659.
Grummer, J. A., L. B. Beheregaray, L. Bernatchez, B. K. Hand, G. Luikart, S. R. Narum, E. B. Taylor. 2019. Aquatic landscape genomics and environmental effects on genetic variation. Trends Ecol. Evol. 34:641-654.
Günther, T. and G. Coop. 2013. Robust identification of local adaptation from allele frequencies. Genetics 195:205-220.
Haller, B. C. and P. W. Messer. 2019. SLiM 3: forward genetic simulations beyond the Wright-Fisher model. Mol. Biol. Evol. 36:632-637.
Hendry, A. P. 2013. Key questions in the genetics and genomics of eco-evolutionary dynamics. Heredity 111:456-466.
Hsu, S. Y. and A. J. W. Hsueh. 2000. Tissue-specific Bcl-2 protein partners in apoptosis: an ovarian paradigm. Physiol. Rev. 80:593-614.
Hsu, S. Y., A. Kaipia, E. McGee, M. Lomeli, and A. J. W. Hsueh. 1997. Bok is a pro-apoptotic Bcl-2 protein with restricted expression in reproductive tissues and heterodimerizes with selective anti-apoptotic Bcl-2 family members. Proc. Natl. Acad. Sci. USA 94:12401-12406.
Huang, J., H. Yu, X. Guan, G. Wang, and R. Guo. 2015. Accelerated dryland expansion under climate change. Nat. Clim. Change 6:166-171. https://doi.org/10.1038/nclimate2837.
Huey, J. A., A. M. Baker, and J. M. Hughes. 2008. The effect of landscape processes upon gene flow and genetic diversity in an Australian freshwater fish, Neosilurus hyrtlii. Freshw. Biol. 53:1393-1408.
Huey, J. A., D. J. Schmidt, S. R. Balcombe, J. C. Marshall, and J. M. Hughes. 2011. High gene flow and metapopulation dynamics detected for three species in a dryland river system. Freshw. Biol. 56:2378-2390.
Hughes, J. M. and M. J. Hillyer. 2006. Mitochondrial DNA and allozymes reveal high dispersal abilities and historical movement across drainage boundaries in two species of freshwater fishes from inland rivers in Queensland, Australia. J. Fish Biol. 68:270-291. https://doi.org/10.1111/j.0022-1112.2006.01073.x.
Jones, F. C., M. G. Grabherr, Y. F. Chan, P. Russell, E. Mauceli, J. Johnson, R. Swofford, M. Pirun, M. C. Zody, S. White, et al. 2012. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484:55-61.
Ke, F., P. Bouillet, T. Kaufmann, A. Strasser, J. Kerr, and A. K. Voss. 2013. Consequences of the combined loss of BOK and BAK or BOK and BAX. Cell Death Dis. 4:e650.
Kingsford, R. T., R. F. Thomas, and A. L. Curtin. 2001. Conservation of wetlands in the Paroo and Warrego River catchments in arid Australia. Pac. Conserv. Biol. 7:21-33.
Kratz, E., P. M. Eimon, K. Mukhyala, H. Stern, J. Zha, A. Strasser, R. Hart, and A. Ashkenazi. 2006. Functional characterization of the Bcl-2 gene family in the zebrafish. Cell Death Differ. 13:1631-1640.
Leigh, C., A. Bush, E. T. Harrison, S. S. Ho, L. Luke, R. J. Rolls, M. E. Ledger. 2015. Ecological effects of extreme climatic events on riverine ecosystems: insights from Australia. Freshw. Biol. 60:2620-2638.
Martin, C. H., J. E. Crawford, B. J. Turner, and L. H. Simons. 2016. Diabolical survival in Death Valley: recent pupfish colonization, gene flow and genetic assimilation in the smallest species range on earth. Proc. R. Soc. B Biol. Sci. 283:20152334.
McCairns, R. J. S., S. Smith, M. Sasaki, L. Bernatchez, and L. B. Beheregaray. 2016. The adaptive potential of subtropical rainbowfish in the face of climate change: heritability and heritable plasticity for the expression of candidate genes. Evol. Appl. 9:531-545.
McGuigan, K., C. E. Franklin, C. Moritz, and M. W. Blows. 2003. Adaptation of rainbow fish to lake and stream habitats. Evolution 57:104-118. https://doi.org/10.1111/j.0014-3820.2003.tb00219.x
McMahon, T. A., R. E. Murphy, M. C. Peel, J. F. Costelloe, and F. H. S. Chiew. 2008. Understanding the surface hydrology of the Lake Eyre Basin: part 2-streamflow. J. Arid Environ. 72:1869-1886. https://doi.org/10.1016/j.jaridenv.2008.06.001
Moldoveanu, T., A. V. Follis, R. W. Kriwacki, and D. R. Green. 2014. Many players in BCL-2 family affairs. Trends Biochem. Sci. 39:101-111.
Morais, R. D. V. S., R. G. Thomé, F. S. Lemos, N. Bazzoli, and E. Rizzo. 2012. Autophagy and apoptosis interplay during follicular atresia in fish ovary: a morphological and immunocytochemical study. Cell Tissue Res. 347:467-478. https://doi.org/10.1007/s00441-012-1327-6
Morais, R. D. V. S., R. G. Thomé, H. B. Santos, N. Bazzoli, and E. Rizzo. 2016. Relationship between bcl-2, bax, beclin-1, and cathepsin-D proteins during postovulatory follicular regression in fish ovary. Theriogenology 85:1118-1131.
Morton, S. R., D. M. Stafford Smith, C. R. Dickman, D. L. Dunkerley, M. H. Friedel, R. R. J. McAllister, J. R. W. Reid, D. A. Roshier, M. A. Smith, F. J. Walsh, et al. 2011. A fresh framework for the ecology of arid Australia. J. Arid Environ. 75:313-329. https://doi.org/10.1016/j.jaridenv.2010.11.001
Mossi, R. and U. Hübscher. 1998. Clamping down on clamps and clamp loaders. Eur. J. Biochem. 254:209-216.
Mossop, K. D., M. Adams, P. J. Unmack, K. L. Smith Date, B. B. M. Wong, and D. G. Chapple. 2015. Dispersal in the desert: ephemeral water drives connectivity and phylogeography of an arid-adapted fish. J. Biogeogr. 42:2374-2388.
Mueller, N., A. Lewis, D. Roberts, S. Ring, R. Melrose, J. Sixsmith, L. Lymburner, A. McIntyre, P. Tan, S. Curnow, et al. 2016. Water observations from space: mapping surface water from 25 years of Landsat imagery across Australia. Remote Sens. Environ. 174:341-352. https://doi.org/10.1016/j.rse.2015.11.003
Murphy, A. L., A. Pavlova, R. Thompson, J. Davis, and P. Sunnucks. 2015. Swimming through sand: connectivity of aquatic fauna in deserts. Ecol. Evol. 5:5252-5264.
Mussmann, S. M., M. R. Douglas, D. D. Oakey, and M. E. Douglas. 2020. Defining relictual biodiversity: conservation units in speckled dace (Leuciscidae: Rhinichthys osculus) of the Greater Death Valley ecosystem. Ecol. Evol. 10:10798-10817.
Narum, S. R., N. R. Campbell, C. C. Kozfkay, and K. A. Meyer. 2010. Adaptation of redband trout in desert and montane environments. Mol. Ecol. 19:4622-4637.
Narum, S. R., N. R. Campbell, K. A. Meyer, M. R. Miller, and R. W. Hardy. 2013. Thermal adaptation and acclimation of ectotherms from differing aquatic climates. Mol. Ecol. 22:3090-3097.
Nearing, J., M. Betka, S. Quinn, H. Hentschel, M. Elger, M. Baum, M. Bai, N. Chattopadyhay, E. M. Brown, S. C. Hebert, et al. 2002. Polyvalent cation receptor proteins (CaRs) are salinity sensors in fish. Proc. Natl. Acad. Sci. USA 99:9231-9236.
Oka, Y. and S. I. Korsching. 2011. Shared and unique G alpha proteins in the zebrafish versus mammalian senses of taste and smell. Chem. Senses 36:357-365.
Pavey, S. A., J. Gaudin, E. Normandeau, M. Dionne, M. Castonguay, C. Audet, L. Bernatchez. 2015. RAD sequencing highlights polygenic discrimination of habitat ecotypes in the panmictic American eel. Curr. Biol. 25:1666-1671.
Peel, M. C., B. L. Finlayson, and T. A. McMahon. 2007. Updated world map of the Köppen-Geiger climate classification. Hydrol. Earth Syst. Sci. Discuss. 11:1633-1644. https://doi.org/10.5194/hess-11-1633-2007
Perrier, C., A. - L. Ferchaud, P. Sirois, I. Thibault, and L. Bernatchez. 2017. Do genetic drift and accumulation of deleterious mutations preclude adaptation? Empirical investigation using RADseq in a northern lacustrine fish. Mol. Ecol. 26:6317-6335.
Peterson, B. K., J. N. Weber, E. H. Kay, H. S. Fisher, and H. E. Hoekstra. 2012. Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS ONE 7:e37135.
Preite, C. K. and R. G. Pearson. 2017. Water-quality variability in dryland riverine waterholes: a challenge for ecosystem assessment. Ann. Limnol. Int. J. Lim. 53:221-232.
Raj, A., M. Stephens, and J. K. Pritchard. 2014. FastSTRUCTURE: variational inference of population structure in large SNP data sets. Genetics 197:573-589.
Rambaut, A., A. J. Drummond, Xie, D., Baele, G. & Suchard, M. A. 2018. Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology. 67:901-904. https://doi.org/10.1093/sysbio/syy032
Raymond, M. and F. Rousset. 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86:248- 249.
Rothschild, L. J. and R. L. Mancinelli. 2001. Life in extreme environments. Nature 409:1092-1101.
Rousset, F. 2008. GENEPOP'007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol. Ecol. Resour. 8:103-106.
Sandoval-Castillo, J., K. Gates, C. J. Brauer, S. Smith, L. Bernatchez, and L. B. Beheregaray. 2020. Adaptation of plasticity to projected maximum temperatures and across climatically defined bioregions. Proc. Natl. Acad. Sci. USA 117:17112-17121.
Sandoval-Castillo, J., N. A. Robinson, A. M. Hart, L. W. S. Strain, and L. B. Beheregaray. 2018. Seascape genomics reveals adaptive divergence in a connected and commercially important mollusc, the greenlip abalone (Haliotis laevigata), along a longitudinal environmental gradient. Mol. Ecol. 27:1603-1620.
Sanford, E. and M. W. Kelly. 2011. Local adaptation in marine invertebrates. Annu. Rev. Mar. Sci. 3:509-535.
Schriever, T. A., M. T. Bogan, K. S. Boersma, M. Cañedo-Argüelles, K. L. Jaeger, J. D. Olden, and D. A. Lytle. 2015. Hydrology shapes taxonomic and functional structure of desert stream invertebrate communities. Freshw. Sci. 34:399-409.
Sheldon, F., S. E. Bunn, J. M. Hughes, A. H. Arthington, S. R. Balcombe, and C. S. Fellows. 2010. Ecological roles and threats to aquatic refugia in arid landscapes: dryland river waterholes. Mar. Freshw. Res. 61:885-895.
Sheldon, F. and C. S. Fellows. 2010. Water quality in two Australian dryland rivers: spatial and temporal variability and the role of flow. Mar. Freshw. Res. 61:864-874.
Smith, S., L. Bernatchez, and L. B. Beheregaray. 2013. RNA-seq analysis reveals extensive transcriptional plasticity to temperature stress in a freshwater fish species. BMC Genomics 14:375.
Smith, S., C. J. Brauer, M. Sasaki, P. J. Unmack, G. Guillot, M. Laporte, L. Bernatchez, and L. B. Beheregaray. 2020. Latitudinal variation in climate-associated genes imperils range edge populations. Mol. Ecol. 29: 4337-4349.
Strickler, A. G. and W. R. Jeffery. 2009. Differentially expressed genes identified by cross-species microarray in the blind cavefish Astyanax. Integr. Zool. 4:99-109.
Sunnucks, P. and D. F. Hales. 1996. Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). Mol. Biol. Evol. 13:510-524.
Syrovatkina, V., K. O. Alegre, R. Dey, and X. - Y. Huang. 2016. Regulation, signaling, and physiological functions of G-Proteins. J. Mol. Biol. 428:3850-3868. https://doi.org/10.1016/j.jmb.2016.08.002
Timms, B. V. 2007. The biology of the saline lakes of central and eastern inland of Australia: a review with special reference to their biogeographical affinities. Hydrobiologia 576:27-37.
Tsujimoto, Y. and S. Shimizu. 2000. Bcl-2 family: life-or-death switch. FEBS Lett. 466:6-10.
Unmack, P. J. 2001. Fish persistence and fluvial geomorphology in central Australia. J. Arid Environ. 49:653-669. https://doi.org/10.1006/jare.2001.0813.
Unmack, P. J., G. R. Allen, and J. B. Johnson. 2013. Phylogeny and biogeography of rainbowfishes (Melanotaeniidae) from Australia and New Guinea. Mol. Phylogen. Evol. 67:15-27.
Vucetich, J. A. and T. A. Waite. 2003. Spatial patterns of demography and genetic processes across the species' range: null hypotheses for landscape conservation genetics. Conserv. Genet. 4:639-645.
Wang, J. 2016. A comparison of single-sample estimators of effective population sizes from genetic marker data. Mol. Ecol. 25:4692-4711.
Williams, W. D. and M. J. Kokkinn. 1988. The biogeographical affinities of the fauna in episodically filled salt lakes: a study of Lake Eyre South, Australia. Hydrobiologia 158:227-236.
Wilson, G. A. and B. Rannala. 2003. Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177-1191.
Wood, J. L. A., M. C. Yates, and D. J. Fraser. 2016. Are heritability and selection related to population size in nature? Meta-analysis and conservation implications. Evol. Appl. 9:640-657.
Youle, R. J. and A. Strasser. 2008. The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 9:47-59.