Speciation accelerated and stabilized by pleiotropic major histocompatibility complex immunogenes
Speciation and the maintenance of recently diverged species has been subject of intense research in evolutionary biology for decades. Although the concept of ecological speciation has been accepted, its mechanisms and genetic bases are still under investigation. Here, we present a mechanism for spec...
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| Published in | Ecology letters Vol. 12; no. 1; pp. 5 - 12 |
|---|---|
| Main Authors | , , , |
| Format | Journal Article |
| Language | English |
| Published |
Oxford, UK
Oxford, UK : Blackwell Publishing Ltd
2009
Blackwell Publishing Ltd Blackwell |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1461-023X 1461-0248 1461-0248 |
| DOI | 10.1111/j.1461-0248.2008.01247.x |
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| Abstract | Speciation and the maintenance of recently diverged species has been subject of intense research in evolutionary biology for decades. Although the concept of ecological speciation has been accepted, its mechanisms and genetic bases are still under investigation. Here, we present a mechanism for speciation that is orchestrated and strengthened by parasite communities acting on polymorphic genes of the immune system. In vertebrates, these genes have a pleiotropic role with regard to parasite resistance and mate choice. In contrasting niches, parasite communities differ and thus the pools of alleles of the adapted major histocompatibility complex (MHC) also differ between niches. Mate choice for the best-adapted MHC genotype will favour local adaptations and will accelerate separation of both populations: thus immune genes act as pleiotropic speciation genes -'magic traits'. This mechanism should operate not only in sympatric populations but also under allopatry or parapatry. Each individual has a small subset of the many MHC alleles present in the population. If all individuals could have all MHC alleles from the pool, MHC-based adaptation is neither necessary nor possible. However, the typically small optimal individual number of MHC loci thus enables MHC-based speciation. Furthermore, we propose a new mechanism selecting against species hybrids. Hybrids are expected to have super-optimal individual MHC diversity and should therefore suffer more from parasites in all habitats. |
|---|---|
| AbstractList | AbstractSpeciation and the maintenance of recently diverged species has been subject of intense research in evolutionary biology for decades. Although the concept of ecological speciation has been accepted, its mechanisms and genetic bases are still under investigation. Here, we present a mechanism for speciation that is orchestrated and strengthened by parasite communities acting on polymorphic genes of the immune system. In vertebrates, these genes have a pleiotropic role with regard to parasite resistance and mate choice. In contrasting niches, parasite communities differ and thus the pools of alleles of the adapted major histocompatibility complex (MHC) also differ between niches. Mate choice for the best-adapted MHC genotype will favour local adaptations and will accelerate separation of both populations: thus immune genes act as pleiotropic speciation genes -'magic traits'. This mechanism should operate not only in sympatric populations but also under allopatry or parapatry. Each individual has a small subset of the many MHC alleles present in the population. If all individuals could have all MHC alleles from the pool, MHC-based adaptation is neither necessary nor possible. However, the typically small optimal individual number of MHC loci thus enables MHC-based speciation. Furthermore, we propose a new mechanism selecting against species hybrids. Hybrids are expected to have super-optimal individual MHC diversity and should therefore suffer more from parasites in all habitats. Speciation and the maintenance of recently diverged species has been subject of intense research in evolutionary biology for decades. Although the concept of ecological speciation has been accepted, its mechanisms and genetic bases are still under investigation. Here, we present a mechanism for speciation that is orchestrated and strengthened by parasite communities acting on polymorphic genes of the immune system. In vertebrates, these genes have a pleiotropic role with regard to parasite resistance and mate choice. In contrasting niches, parasite communities differ and thus the pools of alleles of the adapted major histocompatibility complex (MHC) also differ between niches. Mate choice for the best‐adapted MHC genotype will favour local adaptations and will accelerate separation of both populations: thus immune genes act as pleiotropic speciation genes –‘magic traits’. This mechanism should operate not only in sympatric populations but also under allopatry or parapatry. Each individual has a small subset of the many MHC alleles present in the population. If all individuals could have all MHC alleles from the pool, MHC‐based adaptation is neither necessary nor possible. However, the typically small optimal individual number of MHC loci thus enables MHC‐based speciation. Furthermore, we propose a new mechanism selecting against species hybrids. Hybrids are expected to have super‐optimal individual MHC diversity and should therefore suffer more from parasites in all habitats. Speciation and the maintenance of recently diverged species has been subject of intense research in evolutionary biology for decades. Although the concept of ecological speciation has been accepted, its mechanisms and genetic bases are still under investigation. Here, we present a mechanism for speciation that is orchestrated and strengthened by parasite communities acting on polymorphic genes of the immune system. In vertebrates, these genes have a pleiotropic role with regard to parasite resistance and mate choice. In contrasting niches, parasite communities differ and thus the pools of alleles of the adapted major histocompatibility complex (MHC) also differ between niches. Mate choice for the best-adapted MHC genotype will favour local adaptations and will accelerate separation of both populations: thus immune genes act as pleiotropic speciation genes--'magic traits'. This mechanism should operate not only in sympatric populations but also under allopatry or parapatry. Each individual has a small subset of the many MHC alleles present in the population. If all individuals could have all MHC alleles from the pool, MHC-based adaptation is neither necessary nor possible. However, the typically small optimal individual number of MHC loci thus enables MHC-based speciation. Furthermore, we propose a new mechanism selecting against species hybrids. Hybrids are expected to have super-optimal individual MHC diversity and should therefore suffer more from parasites in all habitats. [PUBLICATION ABSTRACT] Speciation and the maintenance of recently diverged species has been subject of intense research in evolutionary biology for decades. Although the concept of ecological speciation has been accepted, its mechanisms and genetic bases are still under investigation. Here, we present a mechanism for speciation that is orchestrated and strengthened by parasite communities acting on polymorphic genes of the immune system. In vertebrates, these genes have a pleiotropic role with regard to parasite resistance and mate choice. In contrasting niches, parasite communities differ and thus the pools of alleles of the adapted major histocompatibility complex (MHC) also differ between niches. Mate choice for the best-adapted MHC genotype will favour local adaptations and will accelerate separation of both populations: thus immune genes act as pleiotropic speciation genes--'magic traits'. This mechanism should operate not only in sympatric populations but also under allopatry or parapatry. Each individual has a small subset of the many MHC alleles present in the population. If all individuals could have all MHC alleles from the pool, MHC-based adaptation is neither necessary nor possible. However, the typically small optimal individual number of MHC loci thus enables MHC-based speciation. Furthermore, we propose a new mechanism selecting against species hybrids. Hybrids are expected to have super-optimal individual MHC diversity and should therefore suffer more from parasites in all habitats.Speciation and the maintenance of recently diverged species has been subject of intense research in evolutionary biology for decades. Although the concept of ecological speciation has been accepted, its mechanisms and genetic bases are still under investigation. Here, we present a mechanism for speciation that is orchestrated and strengthened by parasite communities acting on polymorphic genes of the immune system. In vertebrates, these genes have a pleiotropic role with regard to parasite resistance and mate choice. In contrasting niches, parasite communities differ and thus the pools of alleles of the adapted major histocompatibility complex (MHC) also differ between niches. Mate choice for the best-adapted MHC genotype will favour local adaptations and will accelerate separation of both populations: thus immune genes act as pleiotropic speciation genes--'magic traits'. This mechanism should operate not only in sympatric populations but also under allopatry or parapatry. Each individual has a small subset of the many MHC alleles present in the population. If all individuals could have all MHC alleles from the pool, MHC-based adaptation is neither necessary nor possible. However, the typically small optimal individual number of MHC loci thus enables MHC-based speciation. Furthermore, we propose a new mechanism selecting against species hybrids. Hybrids are expected to have super-optimal individual MHC diversity and should therefore suffer more from parasites in all habitats. |
| Author | Eizaguirre, Christophe Milinski, Manfred Lenz, Tobias L. Traulsen, Arne |
| Author_xml | – sequence: 1 fullname: Eizaguirre, Christophe – sequence: 2 fullname: Lenz, Tobias L – sequence: 3 fullname: Traulsen, Arne – sequence: 4 fullname: Milinski, Manfred |
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| Keywords | Pleiotropy Vertebrata Hybrids Geographic distribution Major histocompatibility system Hybrid Parasite Sympatry parasites svmpatric speciation major histocompatibility complex Speciation |
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Complex MHC-base 1991; 352 2004; 121 2002; 56 2004; 163 2006; 37 2003; 57 1999; 284 2004; 5 2003; 18 1999; 400 1998; 353 1990; 344 2003; 54 2001; 268 2007; 38 1977 2003b; 16 1990; 44 1989; 31 1982; 218 2001 2000 2005; 102 2000; 403 2002; 420 1981; 35 2009; 364 2001; 16 2007; 2 2002; 108 2000; 287 2007; 20 1998; 52 2006b; 60 2008; 275 1992; 89 1993; 252 2001; 411 1981; 78 2001; 414 1990; 30 1982; 36 1976; 144 2005; 272 2008; 17 2006; 19 2001; 409 1994 2004 2008; 11 1985; 227 2003 2006; 2 2003a; 301 2004; 306 1996; 10 2003; 31 2007; 16 2004; 429 2003; 78 1966; 100 2006a; 273 2003; 425 1986; 324 2004; 17 2004; 58 2005; 8 2004; 271 2007; 274 1999; 153 1992; 139 1963 1969; 26 1996; 351 2005; 2 2005; 59 2003; 62 2005; 17 1990; 8 1995; 260 1992; 63 2005; 14 e_1_2_9_75_1 e_1_2_9_31_1 e_1_2_9_52_1 e_1_2_9_73_1 e_1_2_9_79_1 e_1_2_9_10_1 e_1_2_9_35_1 e_1_2_9_56_1 e_1_2_9_77_1 e_1_2_9_12_1 e_1_2_9_33_1 e_1_2_9_54_1 e_1_2_9_90_1 e_1_2_9_92_1 e_1_2_9_71_1 e_1_2_9_14_1 e_1_2_9_39_1 e_1_2_9_16_1 e_1_2_9_37_1 e_1_2_9_58_1 e_1_2_9_18_1 e_1_2_9_41_1 e_1_2_9_64_1 e_1_2_9_87_1 e_1_2_9_20_1 e_1_2_9_62_1 e_1_2_9_89_1 e_1_2_9_22_1 e_1_2_9_45_1 e_1_2_9_68_1 e_1_2_9_83_1 e_1_2_9_24_1 e_1_2_9_43_1 e_1_2_9_66_1 e_1_2_9_8_1 e_1_2_9_6_1 e_1_2_9_81_1 Wegner K.M. (e_1_2_9_85_1) 2004 e_1_2_9_4_1 e_1_2_9_60_1 e_1_2_9_2_1 Schluter D. (e_1_2_9_74_1) 2000 Ridley M. (e_1_2_9_67_1) 2003 e_1_2_9_26_1 e_1_2_9_49_1 e_1_2_9_47_1 e_1_2_9_53_1 e_1_2_9_51_1 e_1_2_9_72_1 e_1_2_9_11_1 e_1_2_9_34_1 e_1_2_9_57_1 e_1_2_9_78_1 e_1_2_9_13_1 e_1_2_9_32_1 e_1_2_9_55_1 e_1_2_9_91_1 e_1_2_9_93_1 e_1_2_9_70_1 Mayr E. (e_1_2_9_50_1) 1977 e_1_2_9_15_1 e_1_2_9_38_1 e_1_2_9_17_1 e_1_2_9_59_1 e_1_2_9_19_1 e_1_2_9_42_1 e_1_2_9_63_1 e_1_2_9_88_1 e_1_2_9_40_1 e_1_2_9_61_1 Gavrilets S. (e_1_2_9_28_1) 2005; 59 e_1_2_9_21_1 e_1_2_9_46_1 e_1_2_9_84_1 e_1_2_9_23_1 e_1_2_9_44_1 e_1_2_9_65_1 e_1_2_9_86_1 e_1_2_9_7_1 Janeway C.A. (e_1_2_9_36_1) 2001 e_1_2_9_80_1 e_1_2_9_5_1 e_1_2_9_82_1 e_1_2_9_3_1 Haldane J.B.S. (e_1_2_9_30_1) 1992; 63 e_1_2_9_9_1 e_1_2_9_25_1 Schluter D. (e_1_2_9_76_1) 1996; 351 e_1_2_9_27_1 e_1_2_9_48_1 e_1_2_9_69_1 e_1_2_9_29_1 |
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| Snippet | Speciation and the maintenance of recently diverged species has been subject of intense research in evolutionary biology for decades. Although the concept of... AbstractSpeciation and the maintenance of recently diverged species has been subject of intense research in evolutionary biology for decades. Although the... |
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| SubjectTerms | alleles allopatry Animal and plant ecology Animal, plant and microbial ecology Animals Biological and medical sciences Ecology Evolutionary biology Fundamental and applied biological sciences. Psychology General aspects Genetic Speciation Genetics Genetics, Population genotype Hybridization, Genetic Hybrids Immune system Immunology loci major histocompatibility complex Major Histocompatibility Complex - genetics Major Histocompatibility Complex - immunology mating behavior Mating Preference, Animal Models, Genetic Niches Parasite resistance parasites Parasites - immunology parasitology pleiotropy Selection, Genetic Speciation sympatric speciation sympatry Taxonomy Vertebrates Vertebrates - genetics Vertebrates - immunology Vertebrates - parasitology |
| Title | Speciation accelerated and stabilized by pleiotropic major histocompatibility complex immunogenes |
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