172:
scale. The "rare allele phenomenon" might be an indication of this process. Even with the continuous effect of relatively strong endogenous selection against hybrids, a hybrid population might be an example where selection against reproductive isolation results in creating variable recombinant genotypes. Sometimes, this phenomenon might assist in creating a complex of adaptive traits that lead to adaptive novelty.
138:
against poorly fit multilocus genotypes. Therefore, the hybrizymes that increase in frequency could be modifier alleles or genetic markers that increase via hitchhiking. It is not excluded that the targets of selection are the barrier loci, loci that resist homogenization with the other genome during gene flow among diverging species, making them the most different parts of the
171:
With the continual selection against hybrid disadvantage, crossing-over might, over time, interrupt existing linkages and establish new. This generates a shift in selection pressure on loci which are in linkage with these genes and will contribute to further changes in allele frequencies on a genome
128:
Several hypotheses have been proposed to account the high frequency of hybrizymes in hybrid zones such as genetic drift, elevated rates of nucleotide substitutions. or positive selection on alleles which are mildly deleterious in parental taxa. Still, some faced a certain degree of unpredictability;
77:
Early studies focused on detecting electromorphs for loci that code regulatory and non-regulatory enzymes from several functional classes using allozyme electrophoresis and usually involved loci that were polymorphic in parental populations. The phenomenon has also been detected in a broad range of
145:
If allelic variation at these loci is considered, there might be alleles that have differential effect on reproductive isolation or hybrid disadvantage, leading to selection of those who have lower severity. The exact origin and mechanism that maintains these alleles at a high frequency is still a
137:
and hybrid inferiority. In the centre of hybrid zones, the process of constant creation of low-fitness recombinant genotypes will favor any allele that will decrease reproductive isolation, consequently elevating the hybrid fitness. So, a likely mechanism would be negative or purifying selection
112:
Intragenic recombination, under certain circumstances, might create new allelic variants at rates higher than the ones associated with regular mutational processes. Under this hypothesis the variant allele would be a mosaic of the parental alleles. The likelihood of this hypothesis was disputed,
64:
that were observed at high frequency in hybrid zones, but are absent or rare in parental taxa as "the rare allele phenomenon". These alleles can have increased frequencies up to a point of the allele becoming the most common one in the hybrid zone, rendering the term "the rare allele phenomenon"
86:
Multiple hypotheses have been proposed to explain the mutational (molecular) origin of hybrizymes. They include gene conversion, transposable element activity, post-translational modification, mutations. and intragenic recombination. Some of these hypotheses are rejected by research in the past
59:
Originally hybrizymes were defined as "unexpected allelic electromorphs associated with hybrid zones", a formal term proposed by renowned conservation geneticist and biogeographer David S. Woodruff in 1988. By suggesting a new definition for a phenomenon that had been previously widely observed
73:
Hybrid populations display the hybrizyme phenomenon by having increased frequencies of certain alleles that are rare or non-existent outside of the hybrid zone. The hybrizyme phenomenon is widespread in hybrid zones of species of snails, crickets, lizards, salamanders, rodents, fish and birds.
163:
ensures that relatively strong endogenous selection would not quench such potential. Additionally, partial postzygotic reproductive isolation usually involves multiple genes and segregation and recombination of genes creates broadly varying reproductive compatibility in hybrid populations.
113:
through sequencing studies. Although there is yet no specific explanation for hybrizymes, it is not excluded that hybrizymes are generated by the combined effect of recombination and mutation events, with any recombination trace concealed by succeeding mutations. However, research on
39:) meet, mate, and produce hybrid offspring. The hybrizyme phenomenon is widespread and these alleles occur commonly, if not in all hybrid zones. Initially considered to be caused by elevated rates of mutation in hybrids, the most probable hypothesis infers that they are the result of
129:
specifically under the mutational hypothesis the overall substitution rates are elevated and many variants are expected versus having only one allele reaching high frequency and, at the same time, positive selection on deleterious alleles seems ambiguous.
119:
species implies that high recombination rates are possible due to acceleration of genetic variation after hybridization. Furthermore, results are found that indicate that recurrent mutation is unlikely and that support the hypothesis of recombination.
104:. However, the hypothesis has several weaknesses. It does not explain why normally rare alleles are restricted to a hybrid zone, why polymorphic loci are affected more or offers a mechanism that explains the high frequency of even the rarest variants.
95:
Under the mutational hypothesis, hybrizymes likely arise due to simple point mutations. Sequencing data have indicated this and imply low likelihood that hybrizymes arise as a result of transposition or recombination. Research on
132:
Selection does not need to be directed to the hybrizyme, but to other genes with which the hybrizyme is linked, placing genetic hitchhiking in perspective. In other words, hybrid zones are maintained primarily by balance between
158:
Hybridization might expand the prospect of adaptive radiation to the point where positive selection on recombinant hybrid genotypes surpasses the intrinsic selection against them. Therefore, the selection schemes in
87:
couple of years, but there is an unambiguous explanation for the mutational origin of hybrizymes. The two hypotheses most often discussed are increased mutation rates and intragenic recombination.
646:
Hoffman SM, Brown WM (December 1995). "The molecular mechanism underlying the "rare allele phenomenon" in a subspecific hybrid zone of the
California field mouse, Peromyscus californicus".
164:
Consequently, there will be recurrent removal of disadvantageous alleles for reproductive isolation and relative stabilization of hybrid zones, possibly slowing down the path of complete
47:
or infertility). Stated differently, any allele that will decrease reproductive isolation is favored and any linked alleles (genetic markers) also increase their frequency by
920:"Genealogy of the nuclear beta-fibrinogen locus in a highly structured lizard species: comparison with mtDNA and evidence for intragenic recombination in the hybrid zone"
508:
Lammers Y, Kremer D, Brakefield PM, Groenenberg DS, Pirovano W, Schilthuizen M (March 2013). "SNP genotyping for detecting the 'rare allele phenomenon' in hybrid zones".
74:
Intriguingly, the increased frequency of some of these alleles can have a pronounced effect making them 3-20 times more common in hybrids than in non-hybrid populations.
200:
Woodruff DS (March 1989). "Genetic anomalies associated with Cerion hybrid zones: the origin and maintenance of new electromorphic variants called hybrizymes".
463:
150:
analysis of the genomic regions involved in the phenomenon as a more trustworthy pathway to identify genes that impact the level of reproductive isolation.
60:
Woodruff's interpretation bypasses the etiological connotation of alternative terms and avoids inappropriate context. Namely, previous studies referred to
412:"Admixture in European Populus hybrid zones makes feasible the mapping of loci that contribute to reproductive isolation and trait differences"
40:
51:. If the linked alleles used to be rare variants in the parental taxa, they will become more common in the area where the hybrids are formed.
1120:
551:
Hillis DM, Moritz C, Porter CA, Baker RJ (January 1991). "Evidence for biased gene conversion in concerted evolution of ribosomal DNA".
1209:
860:
Golding GB, Strobeck C (1983). "Increased Number of
Alleles Found in Hybrid Populations Due to Intragenic Recombination".
903:
Kanazawa M, Shamoto Y, Aotsuka T (1999). "Amylase3 hybrizyme found in
Japanese freshwater crab, Geothelphusa dehaani".
1008:
Woodruff RC, Lyman RF, Thompson JN (March 1979). "Intraspecific hybridisation and the release of mutator activity".
375:
Smith MF (November 1979). "Geographic variation in genic and morphological characters in
Peromyscus californicus".
147:
486:
464:"Molecular evaluation of interspecific hybrids between Acer albopurpurascens and A. buergerianum var. formosanum"
43:. Namely, in the center of the hybrid zone, negative selection purges alleles against hybrid disadvantage (e.g.
78:
genetic markers such as intron haplotypes, microsatellites, ribosomal DNA spacer variants, and anonymous SNPs.
774:
Schilthuizen M, Hoekstra RF, Gittenberger E (May 2001). "The 'rare allele phenomenon' in a ribosomal spacer".
1173:
Seehausen O (2004). "Response to
Schilthuizen et al.: Hybridization, rare alleles and adaptive radiation".
1017:
725:
655:
560:
817:
Watt WB (November 1972). "Intragenic
Recombination as a Source of Population Genetic Variability".
48:
1041:
990:
949:
877:
842:
799:
689:
533:
478:
392:
357:
283:
44:
596:"Evidence for horizontal transmission of the P transposable element between Drosophila species"
1231:
1205:
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1033:
941:
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791:
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681:
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441:
433:
349:
1182:
1144:
1108:
1075:
1025:
980:
969:"Parallel evolution of an sAat-'hybrizyme'in hybrid zones in Albinaria hippolyti (Boettger)"
931:
869:
826:
783:
743:
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671:
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615:
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568:
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423:
384:
339:
291:
275:
241:
209:
1021:
729:
659:
564:
245:
100:
and
Japanese freshwater crabs confirms that the phenomenon is possibly caused by simple
620:
595:
344:
327:
296:
263:
213:
101:
97:
65:
deceptive. Despite this, these two terms have been used interchangeably in literature.
1225:
787:
748:
713:
994:
846:
803:
693:
537:
482:
361:
1112:
1045:
953:
160:
611:
594:
Daniels SB, Peterson KR, Strausbaugh LD, Kidwell MG, Chovnick A (February 1990).
28:
1186:
1148:
718:
Proceedings of the
National Academy of Sciences of the United States of America
165:
61:
36:
838:
437:
738:
572:
521:
328:"Hybridization between species of the Rana pipiens complex in central Texas"
134:
1156:
1089:
945:
936:
919:
889:
795:
529:
445:
428:
411:
353:
279:
757:
685:
629:
580:
1037:
985:
968:
676:
881:
667:
410:
Lexer, C; Buerkle, C A; Joseph, J A; Heinze, B; Fay, M F (2006-09-20).
396:
32:
24:
1080:
1063:
1029:
462:
Liao PC, Shih HC, Yen TB, Lu SY, Cheng YP, Chiang YC (October 2010).
287:
139:
873:
388:
264:"Selective increase of a rare haplotype in a land snail hybrid zone"
830:
1135:
Seehausen O (April 2004). "Hybridization and adaptive radiation".
232:
Barton NH, Hewitt GM (November 1985). "Analysis of hybrid zones".
115:
20:
1064:"Hybrid zones, barrier loci and the 'rare allele phenomenon'"
311:
Barton NH, Hewwit GM (1981). "Hybrid zones and speciation.".
262:
Schilthuizen M, Hoekstra RF, Gittenberger E (November 1999).
712:
Bradley RD, Bull JJ, Johnson AD, Hillis DM (October 1993).
313:
Evolution and
Speciation: Essays in Honor of M. J. D. White
918:
Godinho R, Mendonça B, Crespo EG, Ferrand N (June 2006).
268:
Proceedings of the Royal
Society B: Biological Sciences
1204:. Sunderland, Massachusetts: Sinauer Associates, Inc.
714:"Origin of a novel allele in a mammalian hybrid zone"
1057:
1055:
769:
767:
19:
is a term coined to indicate novel or normally rare
257:
255:
146:subject of debate and additional studies, such as
1168:
1166:
967:Schilthuizen M, Gittenberger E (September 1994).
31:, geographic areas where two related taxa (e.g.
1103:Elmer KR (2019), "Barrier Loci and Evolution",
707:
705:
703:
641:
639:
195:
193:
191:
189:
187:
185:
503:
501:
499:
227:
225:
223:
8:
1062:Schilthuizen M, Lammers Y (February 2013).
457:
455:
1107:, American Cancer Society, pp. 1–7,
1079:
984:
935:
747:
737:
675:
619:
427:
343:
295:
202:Biological Journal of the Linnean Society
234:Annual Review of Ecology and Systematics
181:
326:Sage RD, Selander RK (December 1979).
7:
246:10.1146/annurev.es.16.110185.000553
345:10.1111/j.1558-5646.1979.tb04763.x
214:10.1111/j.1095-8312.1989.tb00495.x
14:
1175:Trends in Ecology & Evolution
1137:Trends in Ecology & Evolution
788:10.1046/j.1365-294X.2001.01282.x
1068:Journal of Evolutionary Biology
142:between divergent populations.
1113:10.1002/9780470015902.a0028138
648:Journal of Molecular Evolution
41:negative (purifying) selection
1:
510:Molecular Ecology Resources
27:) that are associated with
1248:
1187:10.1016/j.tree.2004.05.011
1149:10.1016/j.tree.2004.01.003
612:10.1093/genetics/124.2.339
148:Next Generation Sequencing
1200:Coyne JA, Orr HA (2004).
108:Intragenic recombination
102:nucleotide substitutions
819:The American Naturalist
739:10.1073/pnas.90.19.8939
573:10.1126/science.1987647
522:10.1111/1755-0998.12044
937:10.1038/sj.hdy.6800823
429:10.1038/sj.hdy.6800898
280:10.1098/rspb.1999.0906
69:Widespread phenomenon
986:10.1038/hdy.1994.129
377:Journal of Mammalogy
124:Cause of maintenance
1022:1979Natur.278..277W
730:1993PNAS...90.8939B
660:1995JMolE..41.1165H
565:1991Sci...251..308H
315:. pp. 109–145.
274:(1434): 2181–2185.
49:genetic hitchhiking
905:Zoological Science
668:10.1007/BF00173198
168:by reinforcement.
45:hybrid inviability
1122:978-0-470-01590-2
1081:10.1111/jeb.12056
776:Molecular Ecology
82:Mutational origin
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1030:10.1038/278277a0
1005:
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988:
964:
958:
957:
939:
915:
909:
908:
900:
894:
893:
857:
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825:(952): 737–753.
814:
808:
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771:
762:
761:
751:
741:
709:
698:
697:
679:
643:
634:
633:
623:
591:
585:
584:
559:(4991): 308–10.
548:
542:
541:
505:
494:
493:
491:
485:. Archived from
468:
459:
450:
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431:
407:
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323:
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154:Adaptive novelty
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1101:
1097:
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1016:(5701): 277–9.
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901:
897:
874:10.2307/2408171
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773:
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724:(19): 8939–41.
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645:
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593:
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550:
549:
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507:
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389:10.2307/1380187
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12:
11:
5:
1245:
1243:
1235:
1234:
1224:
1223:
1218:
1217:
1210:
1192:
1181:(8): 405–406.
1162:
1143:(4): 198–207.
1127:
1121:
1095:
1051:
1000:
959:
910:
895:
852:
831:10.1086/282809
809:
763:
699:
635:
586:
543:
495:
492:on 2020-02-13.
451:
402:
367:
338:(4): 1069–88.
318:
303:
251:
219:
180:
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177:
174:
155:
152:
125:
122:
109:
106:
98:pocket gophers
92:
89:
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67:
56:
53:
13:
10:
9:
6:
4:
3:
2:
1244:
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1211:0-87893-089-2
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1124:
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1110:
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1074:(2): 288–90.
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1069:
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1047:
1043:
1039:
1035:
1031:
1027:
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982:
978:
974:
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947:
943:
938:
933:
930:(6): 454–63.
929:
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921:
914:
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906:
899:
896:
891:
887:
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832:
828:
824:
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813:
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805:
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797:
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782:(5): 1341–5.
781:
777:
770:
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764:
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745:
740:
735:
731:
727:
723:
719:
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687:
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678:
677:2027.42/48050
673:
669:
665:
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657:
654:(6): 1165–9.
653:
649:
642:
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636:
631:
627:
622:
617:
613:
609:
606:(2): 339–55.
605:
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582:
578:
574:
570:
566:
562:
558:
554:
547:
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527:
523:
519:
516:(2): 237–42.
515:
511:
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488:
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480:
477:(4): 413–20.
476:
472:
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458:
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383:(4): 705–22.
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341:
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240:(1): 113–48.
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208:(3): 281–94.
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161:hybrid swarms
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23:variants (or
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1174:
1140:
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1098:
1071:
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1003:
979:(3): 244–8.
976:
972:
962:
927:
923:
913:
904:
898:
868:(1): 17–29.
865:
861:
855:
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812:
779:
775:
721:
717:
651:
647:
603:
599:
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487:the original
474:
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422:(2): 74–84.
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29:hybrid zones
16:
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1202:Speciation
176:References
166:speciation
37:subspecies
862:Evolution
839:0003-0147
471:Bot. Stud
438:0018-067X
332:Evolution
135:gene flow
62:allozymes
55:Etymology
17:Hybrizyme
1232:Genetics
1226:Category
1157:16701254
1090:23324010
995:46527997
973:Heredity
946:16598190
924:Heredity
890:28568015
847:83891085
804:15699880
796:11380889
694:19397913
600:Genetics
538:34785300
530:23241161
483:49576046
446:16985509
416:Heredity
362:11870983
354:28563904
91:Mutation
1046:4255341
1018:Bibcode
954:2834444
882:2408171
758:8415634
726:Bibcode
686:8587112
656:Bibcode
630:2155157
621:1203926
581:1987647
561:Bibcode
553:Science
397:1380187
297:1690333
33:species
25:alleles
1208:
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1088:
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1038:106306
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1010:Nature
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140:genome
1042:S2CID
991:S2CID
950:S2CID
907:: 16.
878:JSTOR
843:S2CID
800:S2CID
749:47476
690:S2CID
534:S2CID
490:(PDF)
479:S2CID
467:(PDF)
393:JSTOR
358:S2CID
288:51606
284:JSTOR
1206:ISBN
1153:PMID
1117:ISBN
1086:PMID
1034:PMID
942:PMID
886:PMID
835:ISSN
792:PMID
754:PMID
682:PMID
626:PMID
577:PMID
526:PMID
442:PMID
434:ISSN
350:PMID
116:Acer
21:gene
1183:doi
1145:doi
1109:doi
1105:eLS
1076:doi
1026:doi
1014:278
981:doi
932:doi
870:doi
827:doi
823:106
784:doi
744:PMC
734:doi
672:hdl
664:doi
616:PMC
608:doi
604:124
569:doi
557:251
518:doi
424:doi
385:doi
340:doi
292:PMC
276:doi
272:266
242:doi
210:doi
35:or
1228::
1179:19
1177:.
1165:^
1151:.
1141:19
1139:.
1115:,
1084:.
1072:26
1070:.
1066:.
1054:^
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1032:.
1024:.
1012:.
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977:73
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940:.
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876:.
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780:10
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