Nusbaumer, David and Garaud, Laura and Ançay, Laurie and Wedekind, Claus (2021) Sex-Specific Stress Tolerance in Embryos of Lake Char (Salvelinus umbla). Frontiers in Ecology and Evolution, 9. ISSN 2296-701X
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Abstract
Sex-Specific Stress Tolerance in Embryos of Lake Char (Salvelinus umbla) David Nusbaumer Laura Garaud Laurie Ançay Claus Wedekind
Salmonid fish have become important models in evolution and ecology, but possible effects of embryo or larval sex are mostly ignored, probably because morphological gonad formation starts only months after hatching and sexual maturation years later. However, recent gene expression studies and first observations in domestic strains suggest that sex-specific life histories could already start at an embryonic stage. Here we test this hypothesis in embryos and larvae of lake char ( Salvelinus umbla ). We sampled wild char and used their gametes to produce embryos of 40 different families. Embryos were raised singly in a stress or a non-stress environment until a late larval stage (stress was induced by allowing remainders of ovarian fluids to support microbial growth). Genetic markers were then used to sex the fish and reconstruct paternity ( N = 1,463, including dead embryos). Primary sex ratio did not differ among families and was about 1:1. Female embryos hatched on average later and showed lower stress tolerance than male embryos. There were significant parental effects on offspring growth and mortality, but the sex differences in embryo performance were not family specific. We conclude that the sexes differ in their life history and susceptibilities to environmental stress already at embryonic stages. Environmental stress during incubation can therefore affect population sex ratio and hence population growth and genetics.
11 17 2021 768263 10.3389/fevo.2021.768263 1 10.3389/crossmark-policy frontiersin.org true Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung http://dx.doi.org/10.13039/501100001711 31003A_159579 31003A_182265 https://creativecommons.org/licenses/by/4.0/ 10.3389/fevo.2021.768263 https://www.frontiersin.org/articles/10.3389/fevo.2021.768263/full https://www.frontiersin.org/articles/10.3389/fevo.2021.768263/full Nat. Rev. Genet. Bachtrog 14 113 2013 Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. 10.1038/nrg3366 J. Stat. Softw Bates 67 1 2015 Fitting linear mixed-effects models using lme4 10.18637/jss.v067.i01 Ecol. Evol. Clark 6 2751 2016 Genetic correlations and little genetic variance for reaction norms may limit potential for adaptation to pollution by ionic and nanoparticulate silver in a whitefish (Salmonidae). 10.1002/ece3.2088 Appl. Geochem. Diez 78 1 2017 High-resolution reconstruction of the 20th century history of trace metals, major elements, and organic matter in sediments in a contaminated area of Lake Geneva, Switzerland. 10.1016/j.apgeochem.2016.12.007 Nature Diggle 450 411 2007 Cooperation and conflict in quorum-sensing bacterial populations 10.1038/nature06279 Mol. Ecol. Feulner 28 615 2019 Genomic insights into the vulnerability of sympatric whitefish species flocks. 10.1111/mec.14977 The Genetical Theory of Natural Selection. Fisher 1930 10.5962/bhl.title.27468 Genetica Forest 144 477 2016 Additive and non-additive genetic components of the jack male life history in Chinook salmon (Oncorhynchus tshawytscha). 10.1007/s10709-016-9917-y Trends Ecol. Evol. Geffroy 34 628 2019 The adaptive sex in stressful environments. 10.1016/j.tree.2019.02.012 J. Fish Biol. Geffroy 97 596 2020 Effects of global warming on sex ratios in fishes. 10.1111/jfb.14429 Freshw. Biol. Giller 60 256 2015 The relationship between individual habitat use and diet in brown trout. 10.1111/fwb.12472 Sex Control in Aquaculture Guiguen 251 Sex determination and sex control in salmonidae Sex Control in Aquaculture Guiguen 35 Sex determination and differentiation in fish: genetic, genomic, and endocrine aspects 10.1002/9781119127291.ch2 Biol. Lett. Immler 10 2014 Sperm variation within a single ejaculate affects offspring development in Atlantic salmon. 10.1098/rsbl.2013.1040 Mol. Ecol. Jacob 19 5296 2010 Effects of different mating scenarios on embryo viability in brown trout. 10.1111/j.1365-294X.2010.04884.x Proc. R. Soc. B Biol. Sci. Jensen 275 2859 2008 Local adaptation in brown trout early life-history traits: implications for climate change adaptability. 10.1098/rspb.2008.0870 Ethology Johnsson 107 587 2001 Sex-specific aggression and antipredator behaviour in young brown trout. 10.1046/j.1439-0310.2001.00682.x Mol. Ecol. Kalinowski 16 1099 2007 Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. 10.1111/j.1365-294X.2007.03089.x Clim. Change Kelly 163 599 2020 Warming winters threaten peripheral Arctic charr populations of Europe. 10.1007/s10584-020-02887-z Ecol. Freshw. Fish Klemetsen 12 1 2003 Atlantic salmon Salmo salar L., brown trout Salmo trutta L. and Arctic charr Salvelinus alpinus (L.): a review of aspects of their life histories. 10.1034/j.1600-0633.2003.00010.x Reprod. Nutr. Dev. Lahnsteiner 35 465 1995 Composition of the ovarian fluid in 4 salmonid species: Oncorhynchus mykiss, Salmo trutta f lacustris, Saivelinus alpinus and Hucho hucho. 10.1051/rnd:19950501 Ecol. Freshw. Fish Louison 25 133 2016 Use of first-order tributaries by brown trout (Salmo trutta) as nursery habitat in a cold water stream network. 10.1111/eff.12197 Genetics and Analysis of Quantitative Traits. Lynch 1998 Sci. Rep. Maitre 7 2017 Sex differentiation in grayling (Salmonidae) goes through an all-male stage and is delayed in genetic males who instead grow faster. 10.1038/s41598-017-14905-9 Biol. Lett. Mari 12 2016 Higher temperature exacerbates the impact of sediments on embryo performances in a salmonid. 10.1098/rsbl.2016.0745 BMC Evol. Biol. Marques da Cunha 19 2019 Low adaptive potential for tolerance to ethynylestradiol, but also low toxicity, in a grayling population (Thymallus thymallus). 10.1186/s12862-019-1558-1 Biol. Lett. Morán 12 2016 The male handicap: male-biased mortality explains skewed sex ratios in brown trout embryos. 10.1098/rsbl.2016.0693 Fish. Manag. Ecol. Nislow 19 451 2012 Towards a life-history-based management framework for the effects of flow on juvenile salmonids in streams and rivers. 10.1111/j.1365-2400.2011.00810.x bioRxiv Nusbaumer Sperm of more colorful males are better adapted to ovarian fluids in lake char (Salmonidae). 10.1101/2021.10.02.462848 Evol. Appl. Nusbaumer 14 462 Testing for population differences in evolutionary responses to pesticide pollution in brown trout (Salmo trutta). 10.1111/eva.13132 Dryad. Nusbaumer Data from: sex-specific stress tolerance in embryos of lake char (Salvelinus umbla). 10.5061/dryad.gqnk98sp3 Guideline for Testing of Chemicals 203 (Fish Acute Toxicity Test). 1992 Nat. Ecol. Evol. Pearse 3 1731 2019 Sex-dependent dominance maintains migration supergene in rainbow trout. 10.1038/s41559-019-1044-6 J. Fish Biol. Pompini 83 404 2013 Temperature-induced sex reversal is not responsible for sex-ratio distortions in grayling Thymallus thymallus or brown trout Salmo trutta. 10.1111/jfb.12174 R: A Language and Environment for Statistical Computing. 2015 Glob. Chang. Biol. Reid 22 682 2016 Global impacts of the 1980s regime shift. 10.1111/gcb.13106 Ecol. Evol. Savary 7 5201 2017 Stocking activities for the Arctic charr in Lake Geneva: genetic effects in space and time. 10.1002/ece3.3073 Nat. Methods Schneider 9 671 2012 NIH Image to ImageJ: 25 years of image analysis. 10.1038/nmeth.2089 BMC Genomics Selmoni 20 2019 Sex-specific changes in gene expression in response to estrogen pollution around the onset of sex differentiation in grayling (Salmonidae). 10.1186/s12864-019-5955-z Philos. Trans. R. Soc. B Biol. Sci. Sutter 375 2020 Within-ejaculate sperm competition. 10.1098/rstb.2020.0066 Ecol. Freshw. Fish Thompson 25 642 2016 Sex-biased survivorship and differences in migration of wild steelhead (Oncorhynchus mykiss) smolts from two coastal Oregon rivers. 10.1111/eff.12242 Freshw. Biol. Tsuboi 58 908 2013 Strategies for the conservation and management of isolated salmonid populations: lessons from Japanese streams. 10.1111/fwb.12096 J. Fish Biol. Turner 60 1570 2002 Ovarian fluid enhances sperm movement in Arctic charr. 10.1111/j.1095-8649.2002.tb02449.x Fish Shellfish Immunol. von Siebenthal 26 531 2009 Tolerance of whitefish embryos to Pseudomonas fluorescens linked to genetic and maternal effects, and reduced by previous exposure. 10.1016/j.fsi.2009.02.008 Conserv. Biol. Wedekind 27 229 2013 Persistent unequal sex ratio in a population of grayling (Salmonidae) and possible role of temperature increase. 10.1111/j.1523-1739.2012.01909.x Ecology Wedekind 91 1251 2010 Elevated resource availability sufficient to turn opportunistic into virulent fish pathogens. 10.1890/09-1067.1 Mol. Ecol. Wilkins 25 4930 2016 Effects of host genetics and environment on egg-associated microbiotas in brown trout (Salmo trutta). 10.1111/mec.13798 Ecol. Evol. Wilkins 7 5082 2017 Environmental stress linked to consumption of maternally derived carotenoids in brown trout embryos (Salmo trutta). 10.1002/ece3.3076 Evol. Appl. Yano 6 486 2013 The sexually dimorphic on the Y-chromosome gene (sdY) is a conserved male-specific Y-chromosome sequence in many salmonids. 10.1111/eva.12032 Data_Sheet_1.PDF 10.3389/fevo.2021.768263.s001 https://www.frontiersin.org/articles/10.3389/fevo.2021.768263/supplementary-material/10.3389/fevo.2021.768263.s001
Item Type: | Article |
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Subjects: | Grantha Library > Multidisciplinary |
Depositing User: | Unnamed user with email support@granthalibrary.com |
Date Deposited: | 30 Jun 2023 05:47 |
Last Modified: | 07 Sep 2024 10:22 |
URI: | http://asian.universityeprint.com/id/eprint/1331 |