a major task for evolutionary biology has been to develop and test theories for the origin of novelty that are consistent with the fundamental genetic principles of gradual populational change .
novelty , however , is a loaded term with many different definitions that include or exclude a variety of morphological characters ( brigandt and love 2012 ) .
following pigliucci ( 2008 ) , we prefer a more inclusive definition of evolutionary novelty : new traits , or novel combinations of traits within a lineage that perform a new ecological function and may result in the establishment of new evolutionary lineages .
more narrowly focused definitions might be desirable for some purposes ( muller and wagner 1991 ; wagner and lynch 2010 ) . however , our goal in this essay is to elaborate one mechanism for the sudden origin and evolutionary success of new variants that applies just as well to exceptional size and shape , new color patterns , use of new habitats , and new exons .
some theorists have invoked special phenomena such as genome - wide  macromutations  ( goldschmidt 1940 ) or  genetic revolutions  ( mayr 1954 ) to get around perceived difficulties with the emergence of profound change as the accumulation of subtle changes by the conventional dynamics of mutation , gene flow , drift and selection . however , modern evolutionary theory and empirical research in genetics have consistently reaffirmed the ability of conventional population genetics to explain the origin of new species and phenotypes , and simultaneously exposed flaws in the alternatives ( charlesworth et al .
for example , goldschmidt ( 1933 , 1940 ) proposed that a novel phenotype ( such as insect wings , a character associated with higher level taxonomy ) must first arise as an instantaneous product of a single  macromutation  or  systemic mutation  .
individuals bearing such macromutations were characterized as  hopeful monsters  by goldschmidt ( 1933 , 1940 ) to emphasize that their appearance is neither purposeful nor gradual , and their prospects for success are a matter of luck .
a hopeful monster is an individual phenotypically discontinuous from the range of phenotypes of its population , and whose hopes of establishing a new lineage lie in finding a novel niche for which its monstrosity happens to be preadapted .
such a mechanism of speciation was criticized early for being so improbable as to  overtax one s credulity  ( dobzhansky 1937 , p. 53 ) because of the rarity of the initial mutation of large effect , and the resulting improbability of finding an equally monstrous mate ( dobzhansky 1937 ) .
recent empirical and theoretical research on hybrid speciation might have revived the hopeful monster in a new , more credible form ( mallet 2007 ) .
recombination of parental chromosomes in the f2 and later generations during hybridization can generate genotypes that express phenotypes outside the normal range of variation observed in either parental gene pool , a phenomenon termed  transgressive segregation 
; rosenthal et al . 2005 ; johnson et al . 2010 ; parsons et al . 2011 ) .
often , transgressive hybrids have higher fitness in novel environments , increasing the likelihood of divergence from parental populations ( arnold and hodges 1995 ; buerkle et al .
2007 ; shahid et al . 2008 ; abbott et al . 2010 ; fitzpatrick et al . 2010 ) .
a few examples of new phenotypes inferred to arise from hybridization include ( see arnold 1997 ; arnold 2006 ; stelkens and seehausen 2009 for more exhaustive reviews ) : extreme size of tiger x lion f1 hybrids ( gray 1954 ) ; unique shapes and colors of hybrid orchids ( rolfe and hurst 1909 ) ; ability of recombinant sunflowers to thrive in extreme habits ( lexer et al .
2003 , 2007 ) ; specialization on a novel host plant in lonicera flies ( schwarz et al .
2005 ) ; and expression of novel gene transcripts ( including new exons ) via alternative splicing in hybrid poplars ( scascitelli et al .
not all specific examples are relevant in nature , and not all would qualify as  evolutionary novelty  under certain definitions ( muller and wagner 1991 ; pigliucci 2008 ; wagner and lynch 2010 ) , but this small selection of cases serves to illustrate sudden appearance of profound differences between parents and hybrid offspring reminiscent of goldschmidt s hopeful monsters.fig . 
1recently metamorphosed juvenile tiger salamanders representative of ambystoma mavortium ( bts ) , a. californiense ( cts ) and transgressive later generation hybrid .
the late generation hybrid has both a transgressive coloration and body size ( mass and snout - vent length ) beyond the range of parental populations recently metamorphosed juvenile tiger salamanders representative of ambystoma mavortium ( bts ) , a. californiense ( cts ) and transgressive later generation hybrid .
the late generation hybrid has both a transgressive coloration and body size ( mass and snout - vent length ) beyond the range of parental populations arnold and colleagues have promoted the importance of transgressive segregation as the  evolutionary novelty  model of hybridization ( arnold 1997 ; arnold et al .
mallet ( 2007 ) even referred to transgressive hybrids as hopeful monsters , and p. bateson ( 1984 , 2002 ) proposed a simple model for the sudden appearance and successful spread of a novel phenotype via hybridization as a mechanism of saltational evolution . we expand and make genetically explicit the haploid , diploid and polyploid cases of his model ( fig .  2 ) .
2003 ) and hybrid fitness ( dobzhansky 1937 ; muller 1942 ; turelli and orr 2000 ) .
all are special cases of a general multilocus model ( fitzpatrick 2008 ) which can give rise to the evolution of novelty or discontinuity as the cumulative or combined outcome of conventional population genetic change .
indeed , recombination has always been recognized as an important source of variation ( mendel 1866 ) ; whether such variation is perceived as profound or 
2genetically explicit versions of bateson s model . a the haploid case , b the diploid case , c allopolyploidy .
genotypes with asterisks are novel recombinant , true - breeding genotypes genetically explicit versions of bateson s model . a the haploid case , b the diploid case , c allopolyploidy .
bateson s ( 1984 , 2002 ) proposal for how recombination can generate sudden change is a straightforward narrative .
two different mutations ( a and b ) appear and become fixed in different populations with similar phenotypes ( circles in his diagram ) .
when the populations merge , recombinant individuals with both a and b express a new phenotype ( diamonds in his diagram ) , which is more successful and becomes fixed . aside from  mutation  , bateson did not use genetically explicit vocabulary , but his diagram suggests a haploid genome , with mutations a and b occurring in different loci such that recombination can place them together in the same individual .
we show a version of bateson s model with explicit haploid , diploid , and allopolyploid cases in fig .  2 .
the key feature is that the new phenotype depends on the interaction between alleles a and b at different loci .
if both a and b alleles are common in the admixed population , the new phenotype will be expressed by a large number of individuals who can interbreed with each other , rather than a single mutant monster with no prospect for a mate . moreover , even if interactions at other loci render some hybrids ( even f1 hybrids ) partly or mostly sterile , recombination could produce transgressive hybrids with restored fertility in the f2 and later generations ( fig . 
.  3a schematic representation of the process by which two fixed allelic differences ( a and b ) at unlinked loci might recombine during meiosis in two f1 hybrids to create a novel homozygous genotype ( aabb ) in the f2 hybrid .
note that the two novel recombinant chromosomes in the f2 are the result of independent recombinational events a schematic representation of the process by which two fixed allelic differences ( a and b ) at unlinked loci might recombine during meiosis in two f1 hybrids to create a novel homozygous genotype ( aabb ) in the f2 hybrid .
note that the two novel recombinant chromosomes in the f2 are the result of independent recombinational events
bateson ( 2002 ) went on to note that his idea had  points of similarity  with the dobzhansky - muller model of hybrid dysfunction ( dobzhansky 1937 ; muller 1942 ; turelli and orr 2000 ) and the earlier verbal model of w. bateson ( 1909 ) .
in fact , the explicit diploid version of bateson s model differs from the dobzhansky - muller model only in the sign of the interaction : the bateson model supposes the interaction between a and b increases fitness , while the dobzhansky - muller model specifies a decrease in fitness of recombinant hybrids ( table  1a , b ) .
both models describe gene interaction ( epistasis ) causing a hybrid phenotype to fall outside the range for either parental population .
that is , they are special cases of transgressive segregation.table  1diploid , two - locus models for hybrid phenotypesaaaaaa(a ) epistatic hybrid dysfunction  bb111  bb11    h01    h1  bb11    h11    h2(b ) epistatic hybrid vigor  bb111  bb11  +  s01  +  s1  bb11  +  s11  +  s2(c ) additive complementation  bb1    2x1    x1  bb1    x11  +  x  bb11  +  x1  +  2xin each case , parental genotypes are aabb aabb .
epistatic hybrid dysfunction ( a : the dobzhansky - muller model ) and epistatic hybrid vigor ( b : the bateson model ) differ only in whether effects are assumed to be deleterious or beneficial .
the additive complementation model ( c ) shows how recombinants can be phenotypically extreme relative to parentals ( aabb and aabb ) even without gene interaction ( each a or b allele contributes an amount x to the phenotypic value , regardless of the other locus ) .
all can be written as special cases of a general quantitative genetic model ( hill 1984 ; lynch and walsh 1997 ; fitzpatrick 2008 ) diploid , two - locus models for hybrid phenotypes in each case , parental genotypes are aabb aabb .
epistatic hybrid dysfunction ( a : the dobzhansky - muller model ) and epistatic hybrid vigor ( b : the bateson model ) differ only in whether effects are assumed to be deleterious or beneficial .
the additive complementation model ( c ) shows how recombinants can be phenotypically extreme relative to parentals ( aabb and aabb ) even without gene interaction ( each a or b allele contributes an amount x to the phenotypic value , regardless of the other locus ) .
all can be written as special cases of a general quantitative genetic model ( hill 1984 ; lynch and walsh 1997 ; fitzpatrick 2008 ) transgressive segregation can also be caused by strictly additive effects of multiple genes ( table  1c ; nilsson - ehle 1911 ; grant 1975 ) .
( 2003 ) because in qtl studies of transgressive hybridization in plants , additive effects are detected more often than epistatic or dominance interactions ( rieseberg et al .
strictly additive and strictly epistatic models are special cases of the general quantitative genetic model allowing phenotypes to be affected by additive , dominance , and epistatic effects ( hill 1984 ; lynch and walsh 1997 ; fitzpatrick 2008 ) .
extending these basic ideas to many loci and multivariate phenotypes leads to the very general conclusion that recombination between disparate genomes has great potential to produce novel phenotypes ( gavrilets 1999 ) .
the primary prediction characterizing many years of speciation research is that hybridization between disparate genomes will often generate novel phenotypes that are inviable or sterile (  hopeless monsters  ) , and this becomes ever more likely with increasing differentiation ( dobzhansky 1937 ; mayr 1942 ; muller 1942 ; orr and turelli 2001 ; coyne and orr 2004 ; gavrilets 2004 ) . at the same time , the number of potentially beneficial interactions might increase ( stelkens and seehausen 2009 ; stelkens et al .
2009 ) , leading to a race between the potential for hybrid speciation and the evolution of complete reproductive isolation . here ,
as in the case of mutations of large effect , there is probably an inverse relationship between the magnitude of a transgressive beneficial phenotype and the likelihood that it will actually be generated in nature .
the most important prediction arising from hybridization as a source of novelty is that admixed populations with many recombinant individuals repeatedly bring together many genetic differences in many unique combinations .
first , instead of a single genetic difference , the diversity of recombinant genotypes after the f1 generation provides a wide field for selection of beneficial versus deleterious interactions ( lexer et al .
2003 ; parsons et al . 2011 ) . as pointed out by arnold and hodges ( 1995 ) , this means that even if most hybrid interactions are deleterious , there is still a good chance for the rare beneficial recombinant to appear , unless f1 hybrids are completely sterile or inviable .
second , segregating hybrid populations will repeatedly produce recombinant genotypes with transgressive phenotypes ( figs .  2 , 3 ) , instead of only producing a single unique mutant or rare variant likely to be lost , even if advantageous ( gillespie 2004 ) .
this means hopeful monsters produced by transgressive segregation have a good chance of finding suitably monstrous mates in a hybrid population and can establish a true - breeding population derived from many independent interspecific matings ( bateson 2002 ) .
although speciation by transgressive hybridization is expected to be rapid in diploids ( ungerer et al .
1998 ) , we predict fixation of novel transgressive hybrids to be more rapid and perhaps more common in haploid and allopolyploid hybrids .
all of the recombinant hybrids in haploid and allopolyploid populations will be true - breeding , compared to just a fraction of diploid recombinant hybrids ( fig .  2 ) .
in the case of complete or incomplete dominance of a and b , all four diploid recombinant genotypes will exhibit a transgressive phenotype , but only the double homozygote will be true - breeding .
this might lead to lower average fitness of a diploid hybrid population that contains some high - fitness transgressive phenotypes for several generations after hybridization is initiated ( johnson et al .
finally , other more subtle predictions might arise from variation in genomic structure and development .
for example , the dobzhansky - muller model helps explain empirical generalizations including haldane s rule and the large - x effect in hybrid dysfunction . by extension
, the expression of beneficial transgressive phenotypes might differ between sex chromosomes and autosomes , with differential consequences for males and females in lineages with chromosomal sex determination . specifically ,
if transgressive phenotypes are often recessive ( s0  <   s1  <   s2 in table  1b ) and one or more of the interacting genes is on the sex chromosome , then the phenotype is more likely to be expressed in the heterogametic sex , even in the f1 generation .
whether such  rules  might exist for transgressive phenotypes depends largely on whether dominance is a consistent effect in trait expression .
the only broad generalization emerging from reviews of the empirical literature so far appears to be that the additive complementation model is often adequate to explain the data ( rieseberg et al .
1999 ; burke and arnold 2001 ) . however , epistasis and dominance are not infrequently detected , and the difference might reflect lower statistical power to detect non - additive effects .
the idea that hybridization can rapidly produce novel forms is familiar among botanists , but rarely appeared in mainstream discussions of speciation until recently thanks to several case studies of homoploid hybrid speciation ( for reviews see : arnold 1997 ; rieseberg et al .
recombination of fixed genetic differences between two populations in the f2 and later generations can produce hybrids with phenotypes novel to both parental populations ( fig . 
3 ) . when these recombinant phenotypes have fitness beyond the range of parental phenotypes they are transgressive ( fig .  1 ) .
bateson s model of hybridogenic hopeful monsters and the dobzhansky - muller incompatibility model of hybrid inviability are both cases of transgressive segregation .
the dobzhansky - muller model produces a  hopeless monster  : hopeless because sterility and inviability make finding a mate and/or novel niche moot and monstrous because sterility and inviability are both phenotypes outside the parental range of phenotypes ( table  1a ) .
the bateson model produces a hopeful monster : hopeful because it has a good chance of finding a mate given continued hybridization and greater fitness than parental phenotypes in some environments , and monstrous because of its transgressive phenotype ( table  1b ) .
all three models are special cases of the general quantitative genetic model , thus reconciling sudden and gradual origins of novelty without requiring a special class of mutations or population dynamics .
transgressive segregation might be an important mechanism promoting sudden phenotypic changes and ecological transitions in evolution .
even if most of the variation produced is deleterious , a rare transgressive hybrid genotype could rapidly fix in a population or establish a novel lineage .
it is even possible that regularities in the distribution of dominance effects could lead to general predictions ( such as the large x effect and haldane s rule ) for transgressive trait expression , but more research on the genetic architecture of transgressive traits is needed .
regardless of those details , admixture can simultaneously bring together many new combinations of alleles , generating multilocus novelties that might never have appeared via gradual accumulation of new mutations in a single population .
gene exchange is not the sole , nor even necessarily most likely , source of evolutionary novelty ( meyer 2002 ; moczek 2008 ) , but is perhaps the most likely mechanism of sudden , population level change .
 the origin of novelty is a critical subject for evolutionary biologists . 
 early geneticists speculated about the sudden appearance of new species via special macromutations , epitomized by goldschmidt s infamous  hopeful monster  . 
 although these ideas were easily dismissed by the insights of the modern synthesis , a lingering fascination with the possibility of sudden , dramatic change has persisted . 
 recent work on hybridization and gene exchange suggests an underappreciated mechanism for the sudden appearance of evolutionary novelty that is entirely consistent with the principles of modern population genetics . 
 genetic recombination in hybrids can produce transgressive phenotypes ,  monstrous  phenotypes beyond the range of parental populations . 
 transgressive phenotypes can be products of epistatic interactions or additive effects of multiple recombined loci . 
 we compare several epistatic and additive models of transgressive segregation in hybrids and find that they are special cases of a general , classic quantitative genetic model . 
 the dobzhansky - muller model predicts  hopeless  monsters , sterile and inviable transgressive phenotypes . the bateson model predicts  hopeful  monsters with fitness greater than either parental population . 
 the complementation model predicts both . 
 transgressive segregation after hybridization can rapidly produce novel phenotypes by recombining multiple loci simultaneously . 
 admixed populations will also produce many similar recombinant phenotypes at the same time , increasing the probability that recombinant  
 hopeful monsters  will establish true - breeding evolutionary lineages . 
 recombination is not the only ( or even most common ) process generating evolutionary novelty , but might be the most credible mechanism for sudden appearance of new forms . 
Revival of the Hopeful Monster
The Bateson Model
The General Model
Predictions
Conclusions