The Hopeful Monster Finds a Mate and Founds a New Species

George Edward Parris




Saltation (fundamental changes in a species in a single-generation) has been argued to be incompatible with evolution and Darwinism.  Indeed, the mental image of a “hopeful monster” looking unsuccessfully for a mate has been used to ridicule the concept put forward by Richard Goldschmidt in 1940.  Nonetheless, over the last decade it has become well known that simple, common pericentric inversions of chromosomes (which may have no effect on morphology) drastically decrease the fertility of affected individuals when mated with individuals with normal centromere parity.  But, mating between individuals with the same (inverted) parity appears to lead to formation of a population with homozygous inverted parity chromosomes, which has normal fertility.  In this paper, it is argued that these populations with homogeneous (pericentromeric) inversions represent nascent new species within larger populations of the parent species.  Examples involving mice, horses and even humans are presented.  The phenotypes of these nascent species are almost indistinguishable from the normal population and they only diverge from the general population through stochastic variation and selection during periods of ecological change.             


species, Goldschmidt, hopeful monster, C3H/HeJ mouse, pericentric inversion


. Grant BR, Grant PR: Fission and fusion of Darwin's finches populations. Philos Trans R Soc Lond B Biol Sci 2008, 363(1505):2821-2829.

. Grant PR, Grant BR: The secondary contact phase of allopatric speciation in Darwin's finches. Proc Natl Acad Sci U S A 2009, 106(48):20141-20148.

. Grant PR, Grant BR, Keller LF, Markert JA, Petren K: Inbreeding and interbreeding in Darwin's finches. Evolution 2003, 57(12):2911-2916.

. Wake DB: Incipient species formation in salamanders of the Ensatina complex. Proc Natl Acad Sci U S A 1997, 94(15):7761-7767.

. Baker RJ, Bradley RD: Speciation in mammals and the genetic species concept. J Mammal 2006, 87(4):643-662.

. Irwin DE, Irwin JH, Price TD: Ring species as bridges between microevolution and speciation. Genetica 2001, 112-113:223-243.

. Grant BR, Grant PR: Lack of premating isolation at the base of a phylogenetic tree. Am Nat 2002, 160(1):1-19.

. Locke DP, Archidiacono N, Misceo D, Cardone MF, Deschamps S, Roe B, Rocchi M, Eichler EE: Refinement of a chimpanzee pericentric inversion breakpoint to a segmental duplication cluster. Genome Biol 2003, 4(8):R50.

. Weise A, Gross M, Schmidt S, Reichelt F, Claussen U, Liehr T: New aspects of chromosomal evolution in the gorilla and the orangutan. Int J Mol Med 2007, 19(3):437-443.

. Kehrer-Sawatzki H, Sandig C, Chuzhanova N, Goidts V, Szamalek JM, Tanzer S, Muller S, Platzer M, Cooper DN, Hameister H: Breakpoint analysis of the pericentric inversion distinguishing human chromosome 4 from the homologous chromosome in the chimpanzee (Pan troglodytes). Hum Mutat 2005, 25(1):45-55.

. Kehrer-Sawatzki H, Szamalek JM, Tanzer S, Platzer M, Hameister H: Molecular characterization of the pericentric inversion of chimpanzee chromosome 11 homologous to human chromosome 9. Genomics 2005, 85(5):542-550.

. Muller S, Finelli P, Neusser M, Wienberg J: The evolutionary history of human chromosome 7. Genomics 2004, 84(3):458-467.

. Szamalek JM, Cooper DN, Hoegel J, Hameister H, Kehrer-Sawatzki H: Chromosomal speciation of humans and chimpanzees revisited: studies of DNA divergence within inverted regions. Cytogenet Genome Res 2007, 116(1-2):53-60.

. Szamalek JM, Goidts V, Chuzhanova N, Hameister H, Cooper DN, Kehrer-Sawatzki H: Molecular characterisation of the pericentric inversion that distinguishes human chromosome 5 from the homologous chimpanzee chromosome. Hum Genet 2005, 117(2-3):168-176.

. Szamalek JM, Goidts V, Searle JB, Cooper DN, Hameister H, Kehrer-Sawatzki H: The chimpanzee-specific pericentric inversions that distinguish humans and chimpanzees have identical breakpoints in Pan troglodytes and Pan paniscus. Genomics 2006, 87(1):39-45.

. Massip K, Bonnet N, Calgaro A, Billoux S, Baquie V, Mary N, Bonnet-Garnier A, Ducos A, Yerle M, Pinton A: Male meiotic segregation analyses of peri- and paracentric inversions in the pig species. Cytogenet Genome Res 2009, 125(2):117-124.

. Demirhan O, Pazarbasi A, Suleymanova-Karahan D, Tanriverdi N, Kilinc Y: Correlation of clinical phenotype with a pericentric inversion of chromosome 9 and genetic counseling. Saudi Med J 2008, 29(7):946-951.

. Bhatt S, Moradkhani K, Mrasek K, Puechberty J, Lefort G, Lespinasse J, Sarda P, Liehr T, Hamamah S, Pellestor F: Breakpoint characterization: a new approach for segregation analysis of paracentric inversion in human sperm. Mol Hum Reprod 2007, 13(10):751-756.

. Collodel G, Moretti E, Capitani S, Piomboni P, Anichini C, Estenoz M, Baccetti B: TEM, FISH and molecular studies in infertile men with pericentric inversion of chromosome 9. Andrologia 2006, 38(4):122-127.

. Martin C, Beaujean N, Brochard V, Audouard C, Zink D, Debey P: Genome restructuring in mouse embryos during reprogramming and early development. Dev Biol 2006, 292(2):317-332.

. Probst AV, Almouzni G: Pericentric heterochromatin: dynamic organization during early development in mammals. Differentiation 2008, 76(1):15-23.

. Rousseaux S, Reynoird N, Escoffier E, Thevenon J, Caron C, Khochbin S: Epigenetic reprogramming of the male genome during gametogenesis and in the zygote. Reprod Biomed Online 2008, 16(4):492-503.

. Talaban R, Sellick GS, Spendlove HE, Howell R, King C, Reckless J, Newbury-Ecob R, Houlston RS: Inherited pericentric inversion (X)(p11.4q11.2) associated with delayed puberty and obesity in two brothers. Cytogenet Genome Res 2005, 109(4):480-484.

. Descipio C, Morrissette JD, Conlin LK, Clark D, Kaur M, Coplan J, Riethman H, Spinner NB, Krantz ID: Two siblings with alternate unbalanced recombinants derived from a large cryptic maternal pericentric inversion of chromosome 20. Am J Med Genet A, 152A(2):373-382.

. Escudero T, Lee M, Stevens J, Sandalinas M, Munne S: Preimplantation genetic diagnosis of pericentric inversions. Prenat Diagn 2001, 21(9):760-766.

. Guardiola MT, Dobin SM, Dal Cin P, Donner LR: Pericentric inversion (12)(p12q13-14) as the sole chromosomal abnormality in a leiomyoma of the vulva. Cancer Genet Cytogenet, 199(1):21-23.

. Guichaoua MR, Gabriel-Robez O, Ratomponirina C, Delafontaine D, Le Marec B, Taillemite JL, Rumpler Y, Luciani JM: Meiotic behaviour of familial pericentric inversions of chromosomes 1 and 9. Ann Genet 1986, 29(3):207-214.

. Liang D, Wu L, Pan Q, Harada N, Long Z, Xia K, Yoshiura K, Dai H, Niikawa N, Cai F et al: A father and son with mental retardation, a characteristic face, inv(12), and insertion trisomy 12p12.3-p11.2. Am J Med Genet A 2006, 140(3):238-244.

. Prontera P, Buldrini B, Aiello V, Rogaia D, Mencarelli A, Gruppioni R, Bonfatti A, Beltrami N, Donti E, Sensi A: Familial pericentric inversion of chromosome 18: intrafamilial variability of the recombinant dup(18q). Genet Couns, 21(1):91-97.

. Ulucan H, Akin R, Kosem M, Gul D: De novo pericentric inversion of chromosome 5 in a girl with mental retardation and unilateral ear malformation. Am J Med Genet A 2006, 140(3):298-299.

. Parris GE: Developmental diseases and the hypothetical Master Development Program. Med Hypotheses, 74(3):564-573.

. Morel F, Laudier B, Guerif F, Couet ML, Royere D, Roux C, Bresson JL, Amice V, De Braekeleer M, Douet-Guilbert N: Meiotic segregation analysis in spermatozoa of pericentric inversion carriers using fluorescence in-situ hybridization. Hum Reprod 2007, 22(1):136-141.

. Chantot-Bastaraud S, Ravel C, Berthaut I, McElreavey K, Bouchard P, Mandelbaum J, Siffroi JP: Sperm-FISH analysis in a pericentric chromosome 1 inversion, 46,XY,inv(1)(p22q42), associated with infertility. Mol Hum Reprod 2007, 13(1):55-59.

. Srebniak M, Wawrzkiewicz A, Wiczkowski A, Kazmierczak W, Olejek A: Subfertile couple with inv(2),inv(9) and 16qh+. J Appl Genet 2004, 45(4):477-479.

. Simard F, Ayala D, Kamdem GC, Pombi M, Etouna J, Ose K, Fotsing JM, Fontenille D, Besansky NJ, Costantini C: Ecological niche partitioning between Anopheles gambiae molecular forms in Cameroon: the ecological side of speciation. BMC Ecol 2009, 9:17.

. Rivera H, Alvarez-Arratia MC, Moller M, Diaz M, Cantu JM: Familial inv(1) (p3500q21.3) associated with azoospermia. Hum Genet 1984, 66(2-3):165-167.

. Goidts V, Armengol L, Schempp W, Conroy J, Nowak N, Muller S, Cooper DN, Estivill X, Enard W, Szamalek JM et al: Identification of large-scale human-specific copy number differences by inter-species array comparative genomic hybridization. Hum Genet 2006, 119(1-2):185-198.

. Gross M, Starke H, Trifonov V, Claussen U, Liehr T, Weise A: A molecular cytogenetic study of chromosome evolution in chimpanzee. Cytogenet Genome Res 2006, 112(1-2):67-75.

. Kehrer-Sawatzki H, Sandig CA, Goidts V, Hameister H: Breakpoint analysis of the pericentric inversion between chimpanzee chromosome 10 and the homologous chromosome 12 in humans. Cytogenet Genome Res 2005, 108(1-3):91-97.

. Fogle TA, McKenzie WH: Cytogenetic study of a large black kindred: inversions, heteromorphisms, and segregation analysis. Hum Genet 1980, 55(3):345-352.

. Baltaci V, Ors R, Kaya M, Balci S: A case associated with Walker Warburg syndrome phenotype and homozygous pericentric inversion 9: coincidental finding or aetiological factor? Acta Paediatr 1999, 88(5):579-583.

. Vine DT, Yarkoni S, Cohen MM: Inversion homozygosity of chromosome no. 9 in a higly inbred kindred. Am J Hum Genet 1976, 28(3):203-207.

. Hoffmann AA, Rieseberg LH: Revisiting the Impact of Inversions in Evolution: From Population Genetic Markers to Drivers of Adaptive Shifts and Speciation? Annu Rev Ecol Evol Syst 2008, 39:21-42.

. Bokma F: Detection of "punctuated equilibrium" by bayesian estimation of speciation and extinction rates, ancestral character states, and rates of anagenetic and cladogenetic evolution on a molecular phylogeny. Evolution 2008, 62(11):2718-2726.

. Lewontin R: The triumph of Stephen Jay Gould. New York Rev Books 2008, 55(2):39-41.

. Parris GE: A hypothetical Master Development Program for multi-cellular orgnisms: Ontogeny and phylogeny. Biosciences Hypotheses 2009, 2:3-12.

. Wilkins JS, Nelson GJ: Tremaux on species: a theory of allopatric speciation (and punctuated equilibrium) before Wagner. Hist Philos Life Sci 2008, 30(2):179-205.

. 48. Zeh DW, Zeh JA, Ishida Y: Transposable elements and an epigenetic basis for punctuated equilibria. Bioessays 2009, 31(7):715-726.

. Futuyma DJ: Evolutionary constraint and ecological consequences. Evolution, 64(7):1865-1884.

. Amemiya CT, Powers TP, Prohaska SJ, Grimwood J, Schmutz J, Dickson M, Miyake T, Schoenborn MA, Myers RM, Ruddle FH et al: Complete HOX cluster characterization of the coelacanth provides further evidence for slow evolution of its genome. Proc Natl Acad Sci U S A, 107(8):3622-3627.

. Carone DM, Longo MS, Ferreri GC, Hall L, Harris M, Shook N, Bulazel KV, Carone BR, Obergfell C, O'Neill MJ et al: A new class of retroviral and satellite encoded small RNAs emanates from mammalian centromeres. Chromosoma 2009, 118(1):113-125.

. Longo MS, Carone DM, Program NCS, Green ED, O'Neill MJ, O'Neill RJ: Distinct retroelement classes define evolutionary breakpoints demarcating sites of evolutionary novelty. BMC Genomics 2009, 10:334.

. Oliver KR, Greene WK: Transposable elements: powerful facilitators of evolution. Bioessays 2009, 31(7):703-714.

. Challem JJ, Taylor EW: Retroviruses, ascorbate, and mutations, in the evolution of Homo sapiens. Free Radic Biol Med 1998, 25(1):130-132.

. Brandt J, Schrauth S, Veith AM, Froschauer A, Haneke T, Schultheis C, Gessler M, Leimeister C, Volff JN: Transposable elements as a source of genetic innovation: expression and evolution of a family of retrotransposon-derived neogenes in mammals. Gene 2005, 345(1):101-111.

. Sciamanna I, Vitullo P, Curatolo A, Spadafora C: Retrotransposons, reverse transcriptase and the genesis of new genetic information. Gene 2009, 448(2):180-186.

. Kapitonov VV, Jurka J: Molecular paleontology of transposable elements in the Drosophila melanogaster genome. Proc Natl Acad Sci U S A 2003, 100(11):6569-6574.

. Mattick JS: Introns: evolution and function. Curr Opin Genet Dev 1994, 4(6):823-831.

. Horie M, Honda T, Suzuki Y, Kobayashi Y, Daito T, Oshida T, Ikuta K, Jern P, Gojobori T, Coffin JM et al: Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature, 463(7277):84-87.

. Shcherbakov VP: Biological species is the only possible form of existence for higher organisms: the evolutionary meaning of sexual reproduction. Biol Direct, 5:14.

. Heng HH: Elimination of altered karyotypes by sexual reproduction preserves species identity. Genome 2007, 50(5):517-524.

. Gonzalez-Forero M: Removing ambiguity from the biological species concept. J Theor Biol 2009, 256(1):76-80.

. Davisson MT, Poorman PA, Roderick TH, Moses MJ: A pericentric inversion in the mouse. Cytogenet Cell Genet 1981, 30(2):70-76.

. Akeson EC, Donahue LR, Beamer WG, Shultz KL, Ackert-Bicknell C, Rosen CJ, Corrigan J, Davisson MT: Chromosomal inversion discovered in C3H/HeJ mice. Genomics 2006, 87(2):311-313.

. Hawes SM, Gie Chung Y, Latham KE: Genetic and epigenetic factors affecting blastomere fragmentation in two-cell stage mouse embryos. Biol Reprod 2001, 65(4):1050-1056.

. Marciniak M, Lenartowicz M, Golas A, Styrna J: Correlation of centromeric heterochromatin C-band polymorphism with breeding failure in mice. Folia Biol (Krakow), 58(3-4):251-255.

. Brooks SA, Lear TL, Adelson DL, Bailey E: A chromosome inversion near the KIT gene and the Tobiano spotting pattern in horses. Cytogenet Genome Res 2007, 119(3-4):225-230.

. Haase B, Jude R, Brooks SA, Leeb T: An equine chromosome 3 inversion is associated with the tobiano spotting pattern in German horse breeds. Anim Genet 2008, 39(3):306-309.

. Santschi EM, Vrotsos PD, Purdy AK, Mickelson JR: Incidence of the endothelin receptor B mutation that causes lethal white foal syndrome in white-patterned horses. Am J Vet Res 2001, 62(1):97-103.

. Vig BK: Sequence of centromere separation: occurrence, possible significance, and control. Cancer Genet Cytogenet 1983, 8(3):249-274.

. Bajnoczky K, Mehes K: Parental centromere separation sequence and aneuploidy in the offspring. Hum Genet 1988, 78(3):286-288.

. Chen FC, Li WH: Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am J Hum Genet 2001, 68(2):444-456.

. Ayala FJ, Coluzzi M: Chromosome speciation: humans, Drosophila, and mosquitoes. Proc Natl Acad Sci U S A 2005, 102 Suppl 1:6535-6542.

. Hey J: Speciation and inversions: chimps and humans. Bioessays 2003, 25(9):825-828.

. Betz JL, Behairy AS, Rabionet P, Tirtorahardjo B, Moore MW, Cotter PD: Acquired inv(9): what is its significance? Cancer Genet Cytogenet 2005, 160(1):76-78.

. Jeong SY, Kim BY, Yu JE: De novo pericentric inversion of chromosome 9 in congenital anomaly. Yonsei Med J, 51(5):775-780.

. Vargas de los Monteros MT, Fernandez-Novoa Garcia MC, Salas Herrero E, San Martin Diez MV, Novales Huertas MA: [Pericentric inversion of chromosome 9. Summary of the authors' results]. An Esp Pediatr 1990, 33(5):442-449.

. Steffensen TS, Gilbert-Barness E, Sandstrom M, Bell JR, Bryan J, Sutcliffe MJ: Extreme variant of enlarged heterochromatin region on chromosome 9Q in a normal child and multiple family members. Fetal Pediatr Pathol 2009, 28(6):247-252.

. Yamada K: Population studies of INV(9) chromosomes in 4,300 Japanese: incidence, sex difference and clinical significance. Jpn J Hum Genet 1992, 37(4):293-301.

. Cotter PD, Babu A, McCurdy LD, Caggana M, Willner JP, Desnick RJ: Homozygosity for pericentric inversions of chromosome 9. Prenatal diagnosis of two cases. Ann Genet 1997, 40(4):222-226.

. Kirin M, McQuillan R, Franklin CS, Campbell H, McKeigue PM, Wilson JF: Genomic runs of homozygosity record population history and consanguinity. PLoS One, 5(11):e13996.


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