Ibridazione naturale e antropogenica Ettore Randi Laboratorio di Genetica ISPRA, sede di Ozzano Emilia (BO) ettore.randi@isprambiente.it Foto Davide Palumbo Foto Giancarlo Tedaldi Images dowloaded for non-profit educational presentation use only
Hybridization Hybridization: interbreeding of individuals from genetically distinct populations, regardless of the taxonomic status of the populations Natural hybridization Anthropogenic hybridization Evolutionary consequences of natural hybridization Conservation issues outbreeding depression destruction of local adaptations generation of new genetic variation adaptive divergence among populations adaptation to anthropogenic changes Assessing hybridization Case studies Morphology Genetics Genomics Wild cats x free-ranging domestic cats Wild wolves x free-ranging (stray) dogs
Natural hybridization and evolution Hybridization: an evolutionarily unimportant process or a widespread and potentially creative evolutionary process? The total weight of evidence contradicts the assumption that hybridization plays a major evolutionary role among higher animals. Successful hybridization is indeed a rare phenomenon among animals. Mayr E. 1963. Animal Species and Evolution. Cambridge, MA, Belknap, p. 133 To be sure, the occasional production of an interspecific hybrid occurs frequently in plants. However, most of these hybrids seem to be sterile, or do not backcross with the parent species for other reasons. Mayr E. 1992. A local flora and the biological species concept. Am. J. Bot. 79: 222 238, p. 233
Hybridization is frequent and important for the evolution of natural populations 1. more than 270 natural hybrid zones 2. more than 50% angiosperms may be of hybrid origins 3. 10% congeneric avian species can hybridize 4. hybridization documented in 23 species of carnivores Lazuli x Indigo bunting
Hybridization & Introgression Introgression: gene flow between populations whose individuals hybridize P1 B1 backcross x F1 F2 hybridization P2 B2 introgression
Allendorf et al. 2001
Passer hispaniolensis Type 1: Natural hybrid taxon Passer domesticus
P. hispaniolensis x P. domesticus = P. italiae X
Distributions of Spanish and House sparrows P. hispaniolensis P. domesticus
Italian sparrow: hybrid zones across the Alps
Natural & apparently neutral introgression in Lepus sp. (nuclear /mtdna discordance; mtdna capture)
Lepus granatensis Lepus castroviejoi
Ranges of hares in the Iberian Peninsula, geographical distribution and frequencies of four mtdna lineages observed in 39 populations Alves et al. Phil. Trans. R. Soc. B 2008;363:2831-2839
Type 3: Natural hybrid zone Natural hybrid zones = tension zones: hybrids were selected against in most hybrid zones = stable hybrid zones: balance between dispersal and selection P1 dispersal dispersal P2 Bombina bombina & B. variegata (Szymura & Barton)
Outbreeding depression fitness reduction in hybrids relative to the parentals
Suture zones: Red-shafted x Yellow-shafted flicker
The flickers (Colaptes auratus) hybrid zone
Northern flickers (Red x Yellow hybrids)
Rose-breasted x Black-headed grosbeak
Bullock x Baltimore oriole
Lazuli x Indigo bunting
Climatic factors (temperature...) maintain the location of avian hybrid zones in a North American suture zone
Anthropogenic hybridization and introgression in conservation genetics
Anthropogenic hybridization Anthropogenic causes of hybridization 1. climate changes: habitat shifts, migration, adaptation 2. habitat changes: modification and destruction 3. chain of extinction: small population size, loss of genetic diversity, inbreeding 4. overkill: hunting, fishery, persecution, poaching 5. introduced species: alien invasive species, feral domesticates Hybridization 1. genetic extinction by hybridization and introgression with native flora and fauna 2. habitat modification break down reproductive isolation 3. loss of genetically distinct populations 4. behavioral changes in wild x domestic hybrids
Type 4: Sterile F1 North American x European mink
Sterile hybrids. Females of the European mink Mustela lutreola hybridize with males from the introduced North American mink M. vison. Embryos are aborted so that hybrid individuals are not detected, but wastage of eggs through hybridization has accelerated decline of the European species [Rozhnov, V.V. (1993) Extinction of the European mink: ecological catastrophe or a natural process? Lutreola 1, 10 16] European mink
Type 6: Complete admixture Merging of hybridizing populations Hybridization and introgression of wild duck species and subspecies with introduced domestic mallard Anas platyrhynchos New Zealand grey duck A. superciliosa superciliosa Australian black duck A. superciliosa rogersi Hawaiian duck A. wyvilliana Florida mottled duck A. fulvigula fulvigula Mexican duck A. platyrhynchos diazi America black duck A. rubripes A conservation problem: massive releases of game-farm mallards threaten endemic wild duck populations
Identification of hybrid individuals Molecular genetic markers: 1. protein electrophoresis (allozymes) 2. DNA markers (PCR; STR) 3. NGSeq (SNPs) mtdna is maternally inherited Y-markers are paternally inherited A first approach to a study of hybridization in animals is to identify populationspecific mtdna and Y haplotypes of the parental populations and to screen suspected hybrid individuals for those haplotypes. Then analyze biparentally inherited nuclear markers: allozymes, microsatellitedna and autosomal SNPs
Fixed alleles in parental populations P1 Hy P2 Diagnostic locus: a locus that is fixed or nearly fixed for different alleles in two hybridizing populations
How many species specific markers are necessary to document the genetic status of individuals from a hybrid zone? Hybrid index
Detecting hybridization: Multivariate analyses Wildcats Domestic cats
Detecting hybridization: Probabilistic models K = 2 migrants mislabelled admixed hybrids
Individual assignment testing admixed migrant q i > 0.80 > 0.90
Conservation genetics of the European wildcat Felis silvestris silvestris
Geographical distribution of wildcat subspecies European African Asian
Genetic distinction (STR, mtdna) of Felis silvestris subspecies Driscoll et al. 2007. The Near Eastern Origin of Cat Domestication. Science
Three cat subspecies in Italy European wildcat F. s. silvestris in peninsular Italy and Sicily African wildcat in Sardinia F. s. libyca Domestic cat F. s. catus domestication c. 11 000 ya
Identification of hybrid cats: Morphology Krüger, M., Hertwig, S. T., Jetschke, G. and Fischer, M. S. (2009). Evaluation of anatomical characters and the question of hybridization with domestic cats in the wildcat population of Thuringia, Germany. Journal of Zoological Systematics and Evolutionary Research, 47: 268 282.
Identification of hybrid cats: Morphology in theory in practice
Wild-living cats in Scotland: wildcats, feral cats or hybrids?
Identification of hybrid cats: Morphometrics Krüger, M., Hertwig, S. T., Jetschke, G. and Fischer, M. S. (2009). Evaluation of anatomical characters and the question of hybridization with domestic cats in the wildcat population of Thuringia, Germany. Journal of Zoological Systematics and Evolutionary Research, 47: 268 282.
Multivariate analysis (PCA) of skull traits wildcats Hybrids? domestic cats
Identification of hybrid cats: Genetics (microsatellites) Wildcats Domestic cats
Identification of hybrid cats: Genetics (microsatellites) A Fc a Fsi Fli B Fc a Fsi Hungary Scotland Fli
PC-II (2.25%) Wildcat hybridization in Italy and in Hungary Hungarian free-living cats Putative hybrids Known hybrids Italian wildcats PC-I (4.83%) Domestic cats M. Pierpaoli et al. 2003. Genetic distinction of wildcat (Felis silvestris) populations in Europe, and hybridization with domestic cats in Hungary. Mol. Ecol.
PC-II (2.25%) Probabilistic identification of hybrid cats Hungarian free-living cats HY60 HY63 HY62 Fsi68 Fsi58 0 Fsi28 3 HY5 9 HY57 Hybrids Fsi228 Fsi284 HY61 Italian wildcats Domestic cats PC-I (4.83%) Domestic cats Italian wildcats Hungarian cats Hybrids
Assignment of individual cats II = 1.0 Italian wildcats HY62 Fsi68 HY60 HY63 Fsi283 HY57 HY59 Fsi580 Fsi228 Fsi284 Hungarian wildcats III = 1.0 Hybrids HY61 Domestic cats I = 1.0
Hybridization in European wildcat populations >40% 8-43% 0-4% 6% 34% 8% >30% 5% 12% 0% 8% 11% (7-35 STR; Structure qw < 0.10-0.20)
Wolf conservation genetics
Conservation genetics of wolves in Italy Population structuring: historical (ESU) vs. recent (MU) isolations Genetic consequences of local bottlenecks Wolf x dog hybridization and gene introgression Depredation, poaching and wolf forensic genetics Wolves = 100 Free-ranging dogs = 1 000 000
Genetic distinction between IT wolves and dogs (STR) 0,6 0,4 0,2 FCA-II 0,0-0,2-0,4 IT wolves -0,6-0,6-0,4-0,2 0,0 0,2 0,4 0,6 0,8 FCA-I Dogs
Coat colour variation in Italian wolves
Detecting wolf x dog hybridization: assignment procedures (Caniglia et al. 2013) Qw = 0.95 dogs IT wolves admixed
Morphological anomalies in wolf x dog hybrids
Hybridization in Baltic wolves (Hindrikson et al. 2012)
Hybridization in Iberian wolves (Godinho et al. 2011) 1 2 3 Hybrid pack in Western Asturias (Spain) 1) Wolf qw = 100% 2) Hybrid qw = 43% = F1? 3) Hybrid qw = 31% = F1- F2?
Wolf x dog hybridization in Europe N Europe (Vilà 2003; Hindrikson 2012) Samples = 1/103 8/74 (Fennoscand, Baltic C., N Russia) = 1% - 11% Markers = 11-18 autosomal STR + Y + mtdna CR Iberia (Godinho 2011) Samples = 8 hybrids / 204 wolves = 4% Markers = 42 autosomal STR + Y + mtdna CR Italy (ISPRA lab; Lorenzini 2013) Samples = 7/107-116/1151 = 6.5% - 10% Markers = 12 39 autosomal STR + Y + mtdna CR
Hybridization: Conclusions Naural hybridization is an important potentially creative process (new species; new genomes) hybrid policy: potential value of hybridized populations hybrids should or should not receive protection? hybrids should be removed (outbreeding depression)? Anthropogenic hybridization is a potential threat to the conservation of genetic diversity in natural populations hybrids of local x alien invasive species wild x feral conspecifics hybridization hybrid detection (F) hybrids will be heterozygous at all loci with population-specific alleles) Is there an acceptable proportion of admixture? Is it possible to select nonhybridized individuals to be used in founding new populations? Should intentional hybridization be used as a tool in conservation (genetic variation and rescue effect)? Evidences of (anthropogenic) adaptive introgression?