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Determinació per factors ambientals de la proporció de sexes a les poblacions: Mecanismes, contribució de la epigenètica i aspectes adaptatius en un context de canvi global
- 1. Francesc Piferrer Seminari Departament d’Ecologia, UB. 19 de febrer de 2016 Determinació per factors ambientals de la proporció de sexes a les poblacions: Mecanismes, contribució de l’epigenètica i aspectes adpatatius en un context de canvi global
- 2. 1.- Sex ratio and sex determination. Environmental factors Outline 2.- Epigenetics. Mechanisms and analytical methods 3.- Application of epigenetics to research in ecology 4.- Epigenomics in natural populations 5.- Adpative aspects in a global change scenario
- 3. “Applied” aspects – Reproductive capacity - Fisheries – Sex control - Aquaculture - Invasive species – Monitoring - Chemical pollution - Climate change “Basic” aspects – Mating competition and sexual selection – Evolution of sex determining mechanims – Sex allocation theory – Speciation
- 4. Penman and Piferrer (2008). Rev. Fish. Sci. 16 (Suppl. 1): 4–34 Major sex factors Minor sex factors Environmental differences monofactorial system polyfactorial system environmental sex determination GSD ESD Sex Determination – Genetic sex determination (GSD) GSD ESD – Environmental sex determination (ESD)
- 5. Environmental Sex Determination (ESD) TSD TSD TSD GSD Warner and Shine (2008). Nature 451, 566-568 Temperature (TSD) pH Population density Photoperiod Hypoxia Salinity … ESD Species with TSD = Natural system in which populations exhibit a direct unambiguous fitness response to thermal fluctuations
- 6. Sex Ratio Response to Temperature in Fish T. min T. max.Nat. Range Temp. Nat. Range Temp. during Develop. Temperature Proportionofmales GSD GSD + Temp. Effects TSD RTD Ospina-Álvarez & Piferrer (2008) PLoS One 3(7): e2837 1. Less TSD species 2. One response pattern 3. Possible effects of cl. change
- 7. The European Sea Bass Temperature and Sex Enigma Sex ratio analysis Fertilization 0 50 100 150 200 250 300 350 TSP Formation of gonadal ridges 35 dpf Increase in PGC number 60-90 dpf First sex-related differences in cyp19a expression 120 dpf Sex differentiation First observable signs of morphological sex differentition 150 dpf Piferrer et al. (2005). Gen. Comp. Endocrinol., 142: 102-110 Dicentrarchus labrax (F. Moronidae). Polyfactorial SD system w. temp. influence G x E interactions.
- 8. Epigenetics “The study of phenomena and mechanisms that cause chromosome- bound, mitotically and/or meiotically heritable changes to gene expression or phenotype that are not dependent on changes to DNA sequence”
- 9. Epigenetic Mechanisms Small RNAs (sncRNA) Long RNAs (lncRNAs) Regulatory RNA Xist, … Monoallelic gene expression miRNA (21-22 nt) Translational repression 3. Non-coding RNAs 1. DNA methylation 2. Histone modifications & Histone variants H3K9me3 repression H3K4me3 activation ON Me Me Me OFFCGATTCGAACG CGATTCGAACG
- 10. Cell membrane Nucleus 2. Epigenetic initiators - DNA binding factors - ncRNAs 3. Epigenetic maintainers - DNA modifying enzymes - Histone modifying enzymmes - Histone variants Environment 1. Epigenators - Temperature - Differentiation signals - Metabolites Signaling (epigenator) pathway ncRNA DNMT HAT DNA-BP HDAC Cytoplasm Genotype Short-term, transient outcomes - transcription - DNA replication & repair Long-term outcomes - chromatin conformation - heritable markers Phenotype Establishment of Epigenetic Marks Genotype + Environment = Phenotype
- 11. Epigenetic Inheritance Cell-cell transfer (mitosis) Organism-organism transfer (meiosis) Multi- vs. transgenerational effects P F1 F2 Multigenerational effects Transgenerational effects F3 P F1 F2 Multigenerational Transgenerational Shao C, et al. (2014) Genome Res. 24:604-15 Inheritance of sexual reversal in tongue sole (ZW/ZZ sex det. system) F1 ZW fish exclusively derived from the paternal pseudo-males ZW offspring develop as pseudo- males without temp. treatment
- 12. R. Margalef (1919–2004) Margalef, 1955.Temperatura, dimensiones y evolución. Publ Inst Biol Apl 19: 13–94 “Merece especial interés la coincidencia entre los carácteres resultantes de una selección (e incluso producción directa: determinación del sexo, poliploidía) de variaciones del genotipo y los que consisten en simples modificaciones o somaciones no hereditarias. Es comprensible que la observación de este paralelismo haya sido tomada como argumento a favor del lamarckismo, aunque sin dar una explicación racional que justifique su asimilación”.
- 13. Methylation(%) Low Temp. High Temp. a b c c 14 8 9 9 MalesFemales 100 50 0 environment DNA methylation gene expression phenotype * * * cyp19a +SF1 cyp19a +Foxl2 cyp19a +SF1 +Foxl2 Ctrl cyp19aLuciferaseActivity 0 2 4 6 8 10 12 14 16 18 Control Methylated * Foxl2 Sf-1 cyp19a Foxl2 Sf-1 cyp19a Males > Females An Epigenetic Switch Linking Temperature and cyp19a Expression Temperature group Low High cyp19a(RQ) 0 2 4 6 8 10 Methylation (%) 0 20 40 60 80 cyp19a(RQ) 0 5 10 15 20 Females only a b r2 = 0.3 P = 0.01 Navarro-Martín et al. (2011). PLoS Genet 7(12): e1002447
- 14. J. Experimental Zoology AquaculturePLoS Genetics Science Time Patent Private company
- 15. Matsumoto et al. (2013). PLoS ONE 8(6): e63599 Red-eared slider turtle (Trachemys scripta) 26°C cyp19a1 hyperMe 100% males 31% cyp19a1 hypoMe 100% females Does a similar mechanism operate in reptiles with TSD? Thermosensitive period Sex differentiation period Thermosensitive period Sex differentiation period FISH REPTILES
- 16. Individual variation in ecologically important traits Evolutionarily important • Provides the raw material for natural selection • Conditions the evolutionary trajectory of populations • Shapes the demographic structure of populations • Affects the dynamics of populations and communities Ecologically important Contribution of Epigenetics to Ecological Research
- 17. How Epigenetics Integrates Genetic and Environmental Information After Bossdorf et al 2008. Ecol Lett.11: 106–115 Alter ECOLOGICAL EPIGENETICS Regulates Epigenetic variation Alters Affects Gene expression Phenotypic variation Ecological interactions Natural selection Genetic variation Affects Affects Through Alters ECOLOGICAL GENETICS Affects
- 18. Morán & Pérez-Figueroa, 2011. BMC Genetics 12:86 Circles – River Tea Triangles – River Ulla Genetic (AFLP) Epigenetic, liver (MS-AFLP) Epigenetic, gonads (MS-AFLP) Open – Immature Filled – Mature Extent and Structure of Epigenetic Variation within and among Natural Populations VP = VG + VE + VGE VG = VA + VD + VI VG = VA + VD + VI + VEpi
- 19. Abiotic factors: Thermal stress Nutrients Light Water What is the relative importance of epigenetic variation in determining the outcome of abiotic and biotic interactions? Biotic interactions: Competition Resistance to predators Resistance to pathogens Herrera & Bazaga 2011. Mol Ecol. 20: 1675–1688 Effects of herbivory on Viola cazorlensis Model 4 Genotype Phenotype Epiphenotype Model 3 Genotype Epiphenotype Phenotype Model 2 Genotype Phenotype Epiphenotype Model 1 Genotype Epiphenotype Phenotype
- 20. Epigenetics Has a Long Way to Go in Ecology Topic 22/04/2013 14/02/2016 % increase Cancer 2675 4563 71 Development 2250 4252 89 Genetics 650 1127 73 Evolution 400 719 80 Animal production 60 76 27 Neurobiology 40 61 53 Ecology 30 58 93 0 500 1000 1500 2000 2500 3000 3500 4000 4500 5000 22/04/2013 14/02/2016
- 21. Individual variation in ecologically important traits Evolutionarily important • Provides the raw material for natural selection • Conditions the evolutionary trajectory of populations • Shapes the demographic structure of populations • Affects the dynamics of populations and communities Ecologically important Individual Variation in Ecologically Important Traits production Production artificial performance Production
- 22. 2. Epigenetics and Animal Production Growth, Product quality, Health, Welfare, Reproduction gamete development fertilization embryonic development Post-hatch/birth development. Internal External ExternalExternal Environmental influences (biotic and abiotic) Fertilization Internal Early develop. Internal
- 23. Effects of early environment in the sea bass Illes Medes natural reserve Experimental Aquarium facility Size of genome (Mb) 675 Genes with description 25,433 Number of CpG sites 10,325,421 % of CpGs 1.53 % Cs in CG context 7.66 Number of CpG islands 30,391 Tine et al. (2014). Nature Comm. 5:5770. Wild sea bass vs. Famed sea bass (NT or HT) DNA methylation – RRBS Histone modification – ChIP Gene expression – RNA-seq Tissues
- 25. H-O Pörtner & Peck 2011 Encyclopedia of Reproduction. • Changing water temperatures • Hypoxia events • Ocean acidification • Shifts in hydrodynamics • Sea level rise Effects of Climate Change Organismal Population Community/EcosystemMolecular/Cellular Sex differentiation Behavioral responses Alterations in developmental time Changes in productivity Changes in food-web interactions DNA methylation Gene expression Metabolism Decrements in aerobic performance Larval dispersal
- 26. ncRNA H3K9MeT H3K9DMe Polycomb Epigenetic modification- related genes Sex differentiation- related genes LT HT Long-lasting temperature effects on gene expression Common Temperature Gene expression is altered in 170 dpf sea bass treated with high temperature (HT) during the thermosensitive period (TSP) 0 50 100 150 200 250 300 350 TSP Sex differentiation LT HT Age (dpf) HT LT Díaz & Piferrer. 2015. BMC Genomics 16:679
- 27. Genes upregulated transgenerationally: - Metabolic genes shifts in energy production. - Immune- and stress-responsive genes the second generation of fish to better cope with elevated temperatures. - Genes involved with tissue development and transcriptional regulation - Similar suite of dierentially expressed genes among developmental and transgenerational inheritance - Heat-shock protein genes were surprisingly unresponsive
- 28. Species Pivotal temp. (ºC) Percent of sexes (:) at pivotal temp. + 1.5ºC Percent of sexes (: ) at pivotal temp. + 4ºC Apistogramma spp. (n = 33 sp) 25.3 62 : 38 81 : 19 Hoplosternum littorale 18.8 56 : 44 65 : 35 Limia melanogaster 25.8 57 : 43 68 : 32 Menidia menidia 14.5 61 : 39 75 : 25 Menidia peninsulae 26.6 57 : 43 69 : 31 Odontesthes argentinensis 25.7 60 : 40 76 : 24 Odontesthes bonariensis 24.2 73 : 27 98 : 2 Poeciliopsis lucida 25.6 68 : 32 92 : 8 Pivotal temp. (mean ± S.E.M.) 23.3 ± 1.5 - - Percent males (mean ± S.E.M.) 50.0 61.7 ± 2.1 78.0 ± 4.1 Pivotal temperature in fish species with TSD and predicted sex ratio shifts with temperature increases Ospina-Álvarez & Piferrer (2008) PLoS ONE 3(7): e2837
- 29. Summary/Take home messages - In a global change scenario, epigenetics provide organisms with a source of phenotypic plasticity that can allow adaption to a new environment - The study of variation in natural populations can be greatly benefited if research in ecology integrates epigenetics - The sex ratio is a fundamental parameter in population demography and in many cases is determined by a combination of genetic and environmental factors - Epigenetic mechanisms provide organisms the capability to integrate genomic and environmental information to produce a given phenotype
- 30. Laia Ribas Laia Navarro Natalia Ospina Noèlia Díaz Dafni Anastasiadi Alejandro Valdivieso Susanna Pla Silvia Joly Gemma Fuster Núria Sánchez Paula Gómez Acknowledgments Collaborators: Christopher Bock, Univ. of Vienna Marco Álvarez, Univ Andrés Bello,Chile Luciano di Croce, CRG, Barcelona Paloma Morán, Univ. Vigo 0.285 Project Project Epigen-Aqua Program I-LINK
- 31. differentiation eeppiiggeenneettiiccss LLaammaarrcckk selection environment phenotypic plasticity heritability hybridisation induction Arabidopsis speciation Darwin chromatinglobal change apomixis development memory natural populations DNA sequenceparamutation phenotype ecologyepigenome DNA methylation conservation miRNA evolution epiallelesimprinting variation inheritance maternal effects histones stress interactions transgenerational animal production genotype aquaculture cloning tarantino Waddington non-linealnarrative