sign in sign up
<<
Home , Reticulate evolution, Symbiogenesis

Interciencia ISSN: 0378-1844 [email protected] Asociación Interciencia Venezuela

Pérez, Julio E.; Alfonsi, Carmen; Muñoz, Carlos TOWARDS A NEW EVOLUTIONARY THEORY Interciencia, vol. 35, núm. 11, noviembre, 2010, pp. 862-868 Asociación Interciencia Caracas, Venezuela

Available in: http://www.redalyc.org/articulo.oa?id=33915598013

How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative TOWARDS A NEW EVOLUTIONARY THEORY

Julio E. Pérez, Carmen Alfonsi and Carlos Muñoz

SUMMARY

The need to elaborate a new evolutionary theory is discussed. mechanisms: , , , fusion Several arguments are given to justify a new theory, mainly of and gene fragments, epigenetic mechanisms such as based on present interpretation of different phenomena such methylation of DNA, tool kits, regulatory cis-elements, - as endosymbiosis, reticulate , the modern synthesis of ization and polyploidy. As well as , other sources of embryonic development and evolution (evo-devo), phenotypic must also be included. plasticity, epigenesis, evolvability, and the several evolutionary

HACIA UNA NUEVA TEORÍA DE LA EVOLUCIÓN Julio E. Pérez, Carmen Alfonsi y Carlos Muñoz RESUMEN

Se analiza la necesidad de elaborar una nueva teoría de la varios mecanismos evolutivos: selección natural, flujo génico, evolución. Se señalan varios argumentos para justificar una deriva génica, fusión de genomas y fragmentos génicos, metila- nueva teoría, basados principalmente en la actual interpretación ción de ADN, “cajas de herramientas”, elementos reguladores de diferentes fenómenos tales como endosimbiosis, evolución re- cis, hibridación y poliploidía. Además, se hace necesario incluir ticulada, síntesis moderna del desarrollo y la evolución (evo-de- diversas fuentes de variación, no solamente mutaciones. vo), plasticidad fenotípica, epigénesis, y evolucionabilidad, y de

RUMO A UMA NOVA TEORIA DA EVOLUÇÃO Julio E. Pérez, Carmen Alfonsi e Carlos Muñoz RESUMO

Analisa-se a necessidad de elaborar uma nova teoria da evo- de vários mecanismos evolutivos: seleção natural, fluxo gênico, lução. São apontados vários argumentos para justificar uma deriva gênica, fusão de genomas e fragmentos gênicos, meti- nova teoria, baseados principalmente na atual interpretação de lação de ADN, “caixas de ferramentas”, elementos reguladores diferentes fenômenos tais como endossimbiose, evolução reticu- cis, hibridação e poliploidia. Além disso, é necessário incluir lada, síntese moderna do desenvolvimento e a evolução (evo- diversas fontes de variação, não somente mutações devo), plasticidade fenotípica, epigênese, e evolucionabilidade, e

Introduction nothing more than an ex- tion through the accumula- generations through chromo- trapolation and magnification tion of these somal change– be described How can the synthetic the- of the events that take place changes. These are largely as a small genetic change? ory be defined? In the words within populations and spe- independent of changes in The synthetic theory has of one of its main proponents cies (). the genes affecting external shown great capacity to in- (Mayr, 1963) the synthetic According to Stebbins morphology; thus, morpho- corporate new ideas. For ex- theory maintains that all evo- (1950), another proponent of logically undifferentiated spe- ample, the paper by King lution is due to the accumu- the modern synthesis, the cies may exhibit substantial and Jukes (1969) on neutral- lation of small genetic chang- theory also includes poly- chromosomal differences. ism and genetic drift as a es guided by natural selec- ploidy, translocations, and But, how can polyploidy new evolutionary mechanisms tion, and that transpecific other chromosomal mutations –a case of rapid was titled ‘Non-Darwinian evolution () is that allow reproductive isola- requiring only one or two evolution’, although it seems

KEYWORDS / Endosymbiosis / Epigenetic Changes / Evo-Devo / / / Received: 11/06/2009. Modified: 09/29/2010. Accepted: 10/08/2010.

Julio E. Pérez. M.A. in , Address: Instituto Oceanográ- Carmen Alfonsi. M.Sc. in Ma- Carlos Muñoz. M.Sc. in Ma- University of Kansas, USA. fico de Venezuela, Universidad rine Sciences, IOV-UDO, rine Sciences, IOV-UDO, Ph.D. in Biology, University of de Oriente, Núcleo Sucre, Venezuela. Dr. in Zoology, Venezuela. Professor, Univer- Southampton, UK. Professor, Cumaná, Venezuela. e-mail: Universidad Central de Ven- sidad Arturo Prat, Iquique, Instituto Oceanográfico de [email protected] ezuela. Professor, IOV-UDO, Chile. e-mail: c.munoz@ Venezuela (IOV), Universidad Venezuela. e-mail: calfonsi@ unap.cl de Oriente (UDO), Venezuela. sucre.udo.edu.ve

862 0378-1844/10/11/862-07 $ 3.00/0 NOV 2010, VOL. 35 Nº 11 to have remained firmly evolution ever varied. For confront and overcome cur- light of new advances in mo- within the fold of the syn- him, essentially, it is a theory rent critiques that it loses all lecular biology. In his own thetic theory. On the other of differential rates of evolu- meaning by including every- words: “It would seem justi- hand, Mayr denied that ran- tion; a modification of Dar- thing. However, Gould fied to assert that, so far, no dom genetic drift is an evo- win’s gradualist model, not a (2002) wrote: “Nothing revision of the Darwinian lutionary mechanism. In his saltationist theory. about microevolutionary ge- paradigm has been necessary book What Evolution Is, netic population, or any oth- as a consequence of the spec- Mayr (2001) wrote: “Molecu- Is another evolutionary er aspect of microevolution- tacular discoveries of molec- lar has found that theory needed? ary theory, is wrong or inad- ular biology.” mutations frequently occur in equate at its level. The mod- Pigliucci (2007) indicated which the new allele produc- Modern synthesis current- ern synthesis is incomplete, that there are some major el- es no change in the of ly reigns as the official sci- not incorrect.” ements missing from the the phenotype. Kimura (1983) entific explanation for evolu- Then Ayala (2005) asked: modern synthesis: embryolo- has called the occurrence of tion (teaching evolution in “Is Gould claiming an expan- gy or development biology; such mutations ‘neutral evo- high schools and colleges sion with some modification the role of in the lution’, and other authors means teaching the synthetic of the Modern Synthesis or is evolution of phenotypic nov- have referred to it as non- theory), having great influ- he claiming something more elties or during major transi- Darwinian evolution. Both ence on both our interpreta- ambitious, namely the ad- tions in evolution; knowledge terms are misleading. Evolu- tion of and our vance of a new theory, even related to , pro- tion involves the fitness of understanding of the world. if within the Darwinian tra- teomics, and the other new individuals and populations, Nevertheless, present inter- dition? Gould’s statements, in “-omics” sciences; and sev- not of genes. When a geno- pretation of different phe- the structure and elsewhere, eral important biological phe- type, favored by selection, nomena such as endosymbio- are inconsistent, if not con- nomena, such as phenotypic carries along as hitchhikers a sis, reticulate evolution, the tradictory.” plasticity, the possibility of few newly arisen and strictly modern synthesis of embry- Gould (2002) indicated that evolutionary capacitance, and neutral alleles, it has no in- onic development and evolu- the study of microevolution epigenetic inheritance. Ac- fluence on evolution. This tion (evo-devo), phenotypic provides little, if any, infor- cording to Pigliucci (2007), may be called ‘evolutionary plasticity, evolvability and mation about macroevolution- non-random epigenetic noise’, but it is not evolu- the several evolutionary ary patterns. Macroevolution changes must be the most tion”. mechanisms: natural selec- is autonomous relative to mi- important factor in a new However, in the opinion of tion, gene flow, genetic drift, croevolution. Although Ayala theory of evolution. Epigen- Stebbins and Ayala (1981), fusion of genomes and gene (2005) supported this idea, etic variation, unlike genetic the “selectionist” and the fragments, methylation of he indicated that the study of variation, can be altered di- “neutralist” views of molecu- DNA, tool kits, regulatory microevolutionary phenomena rectly by the environment lar evolution are competing cis-elements, hybridization is important to macroevolu- and may be inherited by fu- hypotheses within the frame- and polyploidy, indicates the tion, because any correct ture generations. Epigenetic work of the synthetic theory necessity to develop a new theory of macroevolution changes offer an additional of evolution. evolutionary theory, a coher- must be compatible with pathway for evolution. Another example of the ent alternative to modern well-established microevolu- incorporation of new ideas synthesis. As well as muta- tionary principles and theo- Elements to be into the synthetic theory is tions, other sources of ge- ries. In these two senses – incorporated in a new that of punctuated equilibri- netic variation must also be identity at the level of events evolutionary theory um, a theory developed by included. (Pérez et al., and compatibility of theo- Eldredge and Gould (1972), 2008). ries– macroevolution cannot a) Evolvability according to which evolution- Gould (1980) pointed out be decoupled from microevo- ary change occurs relatively the necessity for a new evo- lution. This is the ability of bio- rapidly, as compared to lon- lutionary theory that would On the other hand, Ayala logical systems to evolve, the ger periods of relative evolu- include a variety of themes (2005) agreed with the thesis ability of a population to re- tionary stability. Most popu- either ignored or explicitly that macroevolutionary prin- spond to a selective chal- lations experience very little rejected by modern synthesis ciples are not reducible to lenge. According to Grant change for most of their geo- theorists. In his words: “The microevolutionary approach- (2010) the synthetic theory logical history (stasis) fol- modern synthesis, as an ex- es. This does not imply that addresses evolvability in a lowed by rapid evolutionary clusive proposition, has bro- macroevolutionary studies population genetic sense; events. Eldredge and Gould ken down on both of its fun- cannot be incorporated into some populations have more (1972) indicated that the de- damental claims: extrapola- the synthetic theory of evolu- genetic variation than others gree of gradualism proposed tionism (gradual allelic sub- tion. We need to remember and would therefore be ex- by Darwin was virtually non- stitution as a model for all that the modern theory of pected to generate phenotypic existent in the fossil record, evolutionary changes) and evolution is called “synthet- variation at a faster rate. But and that stasis dominates the nearly exclusive reliance on ic” because it incorporates evolvability should not be history of most fossil species. selection leading to adapta- knowledge from diverse au- treated as a distinct trait of However, for Dawkins (1996) tion.” Later, Gould (1982) tonomous disciplines, such as those populations, indepen- mere- added that modern synthesis genetics, ecology, systemat- dent of the underlying ge- ly proposes that the rate of has sometimes been so ics, and . netic variation. evolution varies, and no bi- broadly constructed, usually However, Mayr (2004) saw Evolvability is no longer ologist has ever claimed (not by defenders who wish to no justification for a new seen as a matter of standing Darwin) that the speed of see it as fully adequate to evolutionary theory, even in genetic variance but as a re-

NOV 2010, VOL. 35 Nº 11 863 sult of the propensity to vary duce, or disable the activity transmitted. The phenomenon ity,” dictates the range of that is afforded by the entire of some genes by: a) the ad- has been described in several habitats that a particular gen- genetic architecture (Pigliuc- dition of a methyl group to a plant species, most notably in otype can occupy (Kutschera ci, 2008). cytosine residue, followed by corn. Paramutation produces and Niklas, 2004). It is not known whether a guanine sequence in a CpG a progressive increase of Nussey et al. (2005) indi- the evolution of evolvability dinucleotide (methylation is methylation of cytosine in cated that phenotypic plastic- is the result of natural selec- often associated with reduced the paramutable allele, the ity can evolve under natural tion or a by-product of other gene activity); b) changes in sensitive allele to be silenced selection. A Dutch population evolutionary mechanisms. the chromatine structure (Walker and Panavas, 2001). of great tits (Parus major) This dilemma has profound through chemical modifica- Parental imprinting is an- presents evidence for varia- implications for the under- tions, especially acetylation other example of epigenetic tion in individual plasticity standing of evolution in gen- or methylation of histone inheritance in which certain in the timing of reproduction, eral (Pigliucci, 2008). Earl , which recruit other autosomal genes have seem- and shows that this variation and Deem (2004) have proteins such as transcription ingly unusual inheritance is heritable. Some great tits claimed that evolvability it- factors and repressors that patterns. The consequence of have shifted the timing of self will evolve predictably in together determine the activ- parental imprinting is that egg-laying, this shift giving response to environmental ity state of specific genes or imprinted genes are ex- them an edge over other perturbation. sets of genes; and c) changes pressed as if they were hemi- great tits in dealing with Introduced species offer in the genetic messages tran- zygous, even though there global warming. These birds unique opportunities to study scribed. RNA editing –such are two copies of each of feed their young with cater- evolutionary changes. Such as changing adenosine to these autosomal genes in pillars. If spring arrives ear- changes might be seen in inosine, which is read as each . Furthermore, when lier, caterpillars mature ear- population dynamics as: a) a guanosine– systematically these genes are examined the lier, before tit chicks hatch, time lag in the wake of inva- alters base sequences, result- only changes that are seen leading to a decline in the sions, where initial growth is ing in an entirely new mes- are extra methyl groups pres- birds’ reproductive success. slow; b) the subsequent de- sage (Ho, 2009). ent in certain bases of the However, there is genetic and even of The epigenetic changes imprinted genes’ DNA variation among tits that al- some invaders after an appar- may be heritable through ei- (Ekstrom, 1994). lows for adjustment of the ently successful invasion; c) ther meiosis or A recent study (Crews et egg-laying date. The birds the surprising success of (Bossdorf et al., 2008). If the al., 2007) demonstrated that most able to modify the tim- some exotic species despite term epigenetic inheritance is heritable epigenetic variation ing of egg-laying in response the genetic bottleneck in- used comprehensively to in- can even affect animal be- to earlier spring are more duced by a small population clude mitotic inheritance, havior. When rats are treated successful at reproducing, as size; and d) the morphologi- then some of the mechanisms only once with a toxin (the chicks hatch at a time when cal changes that species fre- underlying phenotypic plas- fungicide vincozolin) that al- their food is most plentiful. quently undergo when intro- ticity may be based on epi- ters DNA methylation, fe- Although there are not yet duced into new regions genesis. But if the term re- males three generations re- enough long-term data to (Pérez et al., 2006). fers exclusively to meiotic moved from the exposure state for sure that great tits Why do some introduced epigenetic inheritance, then discriminate and prefer males are evolving greater pheno- species invade and become does not overlap who do not have a history of typic plasticity –says established, whereas many phenotypic plasticity, as plas- exposure, whereas similarly Nussey– this advantage sug- fail to invade, or persist as ticity is a genotype-specific, epigenetically imprinted gests that, over time, the small, isolated populations? environmentally-induced, and males do not exhibit such more flexible birds may win According to Gilchrist and non-heritable change of the preference. The toxin induces out, and eventually the popu- Lee (2007) one possibility is phenotype (Oliver Bossdorf, the appearance of new im- lation will be better able to a limit on evolvability. personal communication). In printed-like genes that trans- respond to climate changes. this paper the term is re- generationally transmit this b) Epigenesis stricted to the inheritance of altered epigenome to promote d) Evolutionary development epigenetic variation across new phenotypes. (evo-devo) Epigenetic inheritance is generations. As behavior is regarded to the term for heritable chang- The best known examples be the most responsive aspect was es in phenotype not ex- of epigenetics are paramuta- of animal phenotypes, such discussed in detail by Dar- plained by DNA changes. tion and parental imprinting. epigenetic effects on behavior win in The Origin of Spe- Kardong (2003) adopted the Paramutation is a non-Men- may have particularly pro- cies; there is a complete term epigenomics to refer to delian heritable epigenetic found evolutionary conse- chapter dedicated to this top- events that occur above modification in the quences. ic. Darwin (1859) saw that (hence epi-) the level of the that can be passed to the embryonic resemblances DNA (hence genomic). Epig- next generation. It is an in- c) Phenotypic plasticity would be a very strong argu- enomics is the analysis of the teraction between two alleles ment in favor of the connect- normal non-genetic processes of a single locus that results In many the edness of different animal that influence the characteris- in a heritable change of one same genotype can give rise groups. tics of the phenotype during allele. In paramutation, one to many different phenotypic In modern synthesis, how- the lifetime of the . allele affects the other in one variants whose appearance or ever, this important element Epigenetic changes are generation and in future gen- behavior depends on its envi- was missing: how do forms based on biochemical modifi- erations, even if the allele ronmental setting. This phe- change; how do new struc- cations that can activate, re- that causes the change is not notypic variation or “plastic- tures arise? The key to un-

864 NOV 2010, VOL. 35 Nº 11 derstanding how complex different regulatory mecha- that can be easily entered tory changes may be true, it structures arise and evolve nisms may contribute to the into population-dynamic al- is at best premature (Hoek- is development. “Evo-devo” stability of Hox clusters. gorithms, and will not for stra and Coyne, 2008). is the field that unites de- For example, both higher some time. velopmental and evolution- order chromatin structure Furthermore, evo-devo e) Reticulate evolution ary biology, and their sup- and local cis-regulatory ele- aims at explaining how de- porters (Carroll, 2000, 2005; ments may result in coordi- velopment itself evolves and In The Origin of Species, Stern, 2000; Wray, 2007) nated regulation of neigh- how the control of develop- Darwin wrote a chapter en- claim to have revolutionized boring Hox loci. Further- mental processes is brought titled Hybridism, in which the study of both macro- more, in some taxa, most about by the interplay be- he analyzed the causes of and microevolution. notably Drosophila, Hox tween genetic, epigenetic, sterility in hybrids, not hy- Evolutionary developmen- linkage does not appear to and environmental factors. bridization as a possible tal biology is a discipline be required for appropriate Some examples in evo- process of speciation. Nei- concerned with the discov- Hox expression (Ryan et al., devo involve cis-regulatory ther Darwin nor the propo- ery and understanding of 2007). elements (short, noncoding nents of the synthetic theo- the changes in developmen- The Hox genes shape the DNA sequences that control ry developed the idea of tal mechanisms and their number and appearance of expressions of a nearby reticulate evolution as a role in the evolutionary ori- repeated structures along gene). An active debate is mechanism of speciation. gin of aspects of the pheno- the main body axes of ani- currently developing in rela- Currently, there is general type. Ho (2009) indicated mals. Shifts in the expres- tion to these claims. Ac- agreement on the great im- that there is no separation sion of tool-kit genes during cording to Wray (2007) portance of hybridization as between development and development not only ac- there is evidence to support an evolutionary phenomenon evolution, and the organism count for large-scale differ- the claim that cis-regulatory (Chapman and Burke, 2007; actively participates in ences in animal forms; they mutations are more impor- Mallet, 2007). shaping its own develop- can also explain differences tant than structural muta- Reticulate speciation can ment as well as the evolu- among closely related spe- tions in phenotypic evolu- occur through polyploidy tionary future of the entire cies, or even populations of tion. Numerous studies have (allo- and auto-polyploidy) ecological community of the same species. identified cis-regulatory mu- and diploid homoploidy. Al- which it is a part. But, is evo-devo just a tations with functionally though both modes of hy- Extensive studies of em- matter of genes? Are the significant consequences for brid speciation have oc- bryology reveal that despite large evolutionary changes morphology, , and curred in , polyploidy, great differences in appear- in body pattern the result of behavior. The focus has especially through allopoly- ance, almost all animals changes in gene regulation now shifted to considering ploidy, appears to be more share a common “tool kit” due to natural selection? whether cis-regulatory and common than homoploid of body building genes. The How do we explain the lack coding mutations make hybrid speciation, and more best example of tool kit of correlation between ge- qualitatively different con- is known about its overall genes is called Hox genes, netic and morphological dif- tributions to phenotype evo- evolutionary significance. which control segmental ferences between species? lution. In particular, cases Allopolyploidy speciation patterning during develop- Evo-devo is still based on in which parallel mutations can result from somatic ment. The various Hox the old idea that develop- have produced parallel trait chromosome doubling into a genes are situated very ment is dominated by genes modifications suggest that diploid hybrid, followed by close to one another in the in a “genetic programme” of some phenotypic changes selfing to produce a tetra- chromosome, in groups or gene regulation (Ho, 2009). are more likely to result ploid, as in Primula kewen- clusters. It has also been Coyne (2009) indicated that from cis-regulatory muta- sis, an allopolyploid that observed in a phylogeneti- in the past three decades, tions than from coding mu- arose spontaneously in 1909 cally widespread range of virtually all the major ad- tations. among cultivated diploid taxa that the relative spatial vances in evolutionary de- The idea that macroevolu- hybrids of P. verticillata and/or temporal expression velopmental biology, or tion has mainly been the and P. floribunda (Ramsey of Hox genes is correlated “evo-devo,” have been firm- result of changes at cis-reg- and Schemske, 2002). Allo- with their relative position ly grounded in genetics. ulatory sites was first devel- polyploidization results in within Hox clusters. This There must be recognition oped by Carroll (2000, instantaneous speciation be- correspondence between of the important role of epi- 2005) and Stern (2000). On cause any backcrossing to gene expression and cluster genetic signals from the in- the other hand, Hoekstra the diploid parents produces organization has been ternal and external environ- and Coyne (2008) indicated sterile triploid offspring. termed colinearity. ment that activate DNA to that genomic studies show Certainly, allopolyploids The existence of colinear- produce a large alteration in no strong evidence to sup- are a sizable fraction of ity implies that linkage im- form and function. port important cis-regulato- well-studied crop cases, pacts gene regulation. How- The integration of evo- ry changes in evolution. Ad- such as wheat, cotton, ever, Hox colinearity is not devo with the synthetic the- aptations of both form and maize, sugar cane, coffee, universal, and no single ory seems to be difficult. physiology are likely to in- and tobacco. mechanism has been identi- As indicated by Müller volve a mixture of struc- Homoploid hybrid specia- fied that can explain Hox (2007), the inclusion of in- tural and cis-regulator y tion is a normal sexual event colinearity or the persis- formation from developmen- changes, and structural where each gamete has a tence of Hox clusters in di- tal systems will be difficult changes are unlikely to be haploid complement of the verse metazoan lineages. to achieve, as current evo- negligible. Although the from its par- Rather, it seems that several devo does not generate data claim related to cis-regula- ents, but the gametes that

NOV 2010, VOL. 35 Nº 11 865 form the zygote come from duce complex or unpredictable found what seems to be the the initial phase of a transition different species. In this outcomes that are not easily entire genome of a parasitic from free-living organisms to case, both parents have the explained, because they are bacterium, Wolbachia pipien- a nitrogen-fixing plant entity, a same number of chromo- derived from the interactions tis, inserted into the genome transition process which may somes, and successful back- of different proteins encoded of the Drosophila ananassae. mimic what drove the evolu- crossing to the parents is by divergent nucleotide se- The discovery suggests that tion of from a possible, so it is thought that quences from two previously the bacterial genome must cyanobacterial ancestor. The the hybrids have to be iso- isolated parental genomes. Ac- have provided some sort of evolution by symbiotic associa- lated from the parents by cording to Grant-Downton and evolutionary advantage to its tion () is the undergoing selection for Dickinson (2005), an indica- host. most likely model for many in the novel environment. tion that this explanation is Lake (2009) showed evi- evolutionary events that have Diploid hybrid speciation inadequate comes from rare dence that the double-mem- resulted in rapid changes or is much rarer than allopoly- hybrids, where their phenotype brane, Gram-negative prokary- the formation of new species ploidization. Hybrid specia- is always disproportionately otes were formed as a result of of plants (Roossinck, 2005). tion is very common in skewed towards one of the a between an an- -host partnerships, in- some groups of organisms parents; hybridization events in cient Actinobacterium and an cluding genomic fusions, are such as plants, fish, amphib- plants can unlock variations ancient Clostridium. The endo- more common than many bi- ians and some invertebrates, not seen in either parental spe- symbiotic theory envisions the ologists realize, and play an but is virtually absent in cies. evolution of the first eukary- important and underestimated others like mammals and Grant-Downton and Dickin- otic cells to have resulted from role in evolution. Some symbi- most arthropods (Linder et son (2006) indicated that re- the permanent incorporation of ologists have not considered al., 2003). search of the epigenetics of once autonomous, physiologi- as potential symbionts. In relation to homoploidy, allopolyploid hybrids between cally different prokaryotic cells In general, this is the result of Mallet (2007) indicated that, Arabidopsis thaliana and A. incorporated into a host pro- a refusal to see viruses as liv- in plants, about 20 well-es- arenosa to form a stable fer- karyotic cell-type (Kutschera ing organisms. An important tablished homoploid hybrid tile hybrid allotetraploid, A. and Niklas, 2004). According example is the viral-eukaryotic species are known, the best suecica, reveals that the F1 to this concept, mitochondria symbiosis that occurs in the documented examples being hybrids showed a range of evolved from some form of parasitoid wasp-polydnavirus three species of desert sun- phenotypes not necessarily in- ancient aerobic , interactions, in which the virus flowers. Reiseberg (1997) termediate between the par- whereas chloroplasts evolved carries the essential genes re- reproduced in the green- ents. Some of these pheno- from some form of cyanobac- quired to suppress the immune house the formation of a types, such as pigmentation, teria-like . Upon system of the lepidopteran host naturally occurring species were unstable in hybrids, indi- gaining permanent residency of the wasp (Wren et al., of sunflower, Helianthus cating that dynamic epigenetic in their host cell, mitochondria 2006). In many such examples, anomalus, a diploid out- changes affecting gene expres- and chloroplasts continued to the viral genome has been in- crossing species that arose sion had taken place. function and replicate in such tegrated into the wasp ge- from recombinational specia- a manner that derivative con- nome. Once viruses enter a tion. The putative ancestors f) Endosymbiosis and federations were produced genome, their capacity for evo- are H. annus and H. petio- symbiogenesis when the host cell underwent lutionary innovation remains laris, which occur widely in binary (Margulis, persistently active and can in- the western USA and often Endosymbiosis is a relation- 1970). teract with newly arrived ex- form hybrid swarms. These ship in which one organism Zimmer (2009) adds addi- ogenous viruses or with other offspring are largely sterile belonging to one species tional evidence to the endo- genetic components and regu- because the species differ in within another from a different symbiotic hypothesis: genes in latory mechanisms, thus in- fixed chromosome arrange- species in a mutually benefi- mitochondria closely resemble creasing evolutionary plasticity ments, which causes meiotic cial manner. Endosymbiosis is genes in alpha protobacteria, (Lower et al., 1996, cited by difficulties in the heterozy- viewed as a phenomenon for not those in ; and Ryan, 2006). gous hybrids. Over several saltatory evolution and is seen some of the proteins that carry Approximately 8% of the generations, however, these at its most powerful in the out reactions in mitochondria human genome consists of hu- arrangements can sort them- blending of whole genomes are encoded in nuclear DNA. man endogenous retroviruses selves out into a new ge- (Ryan, 2006). Symbiogenesis The closest relatives of these (HERVs), and, if HERV frag- nome that is perfectly com- is the resulting evolutionary genes are among bacterial ments and derivatives are in- patible with others of its change that occurs by perma- genes, not genes. It cluded, the retroviral legacy type but incompatible with nent integration of symbionts. seems that after the ancestors amounts to roughly half our the genomes of its ancestors. Margulis (1981) stated that of mitochondria entered the DNA. A long term conse- In H. anomalus, this chro- all life on is bacterial or ancestors of today’s eukary- quence of the symbiotic viral mosomal sorting was supple- derives, by symbiogenesis, otes, some of their genes got component of the human ge- mented by the fixation of from communities of bacteria; moved into the eukaryote ge- nome is an increase in genetic new rearrangements as well, and Ran et al. (2010) indicated nome. plasticity, which has important as more conventional genetic that an ancient cyanobacterial Ran et al. (2010) sequenced implications in medicine and changes, some of which incorporation into a eukaryotic the genome of a cyanobacte- . Virus- must involve to organism led to the evolution rium residing extracellulary in host integrations probably its peculiar habitat. of (chloroplasts) and symbiosis with the plant Azol- played a key role in the ori- Epigenetics has played an subsequently to the origin of la filiculoides suggesting that gins of both non-adaptive and important role in hybridization the plant kingdom. this cyanobacterial symbiont of adaptive immunity. Retrovi- events. Hybrids frequently pro- Hotopp et al. (2007) have Azolla can be considered at ruses have also been detected

866 NOV 2010, VOL. 35 Nº 11 in the of many differ- tive allele replacement within several evolutionary mecha- think that a new evolutionary ent species of mammals, in- populations. Its implications nisms such as: fusion of ge- theory is needed. cluding non-human primates, for phylogeny are also radi- nomes and gene fragments, cats, mice, and guinea pigs cally different. Nevertheless, methylation of DNA, tool kits, REFERENCES (Ryan, 2007, 2009). both modes of adaptation regulatiory cis-elements, hy- Margulis (1970) proposed drive the evolution of pro- bridization and polyploidy. It Ayala FJ (2005) The structure of that symbiosis, not random karyotes. At the same time, evolutionary theory: on Stephen is also necessary to include Jay Gould’s monumental mas- , was the driving new genes from far away different sources of genetic terpiece. Theol. Sci. 3: 97-117. force behind evolution, and must impart new tempo and variation, not only mutations. Bossdorf O, Richards CL, Pigliucci that cooperation between or- new modes in prokaryotic All this knowledge under- M (2008) Epigenetics for ecolo- ganisms and the environment, evolution. Horizontally trans- scores the necessity to devel- gists. Ecol. Lett. 11: 106-115. rather than competition ferred genes, because they op a new evolutionary theory, Carroll SB (2000) Endless forms: among individuals, was the can confer radically new and a coherent alternative to mod- the evolution of gene regula- chief agent of natural selec- complex phenotypes, might ern synthesis. tions and morphological diver- tion. She stated that “Dar- often result in adaptive radia- Evolution can occur incre- sity. Cell 101: 577-580. win’s great vision was not tions and the formation of mentally through small chang- Carroll SB (2005) Evolution at two levels: on genes and form. wrong, only incomplete.” The new subpopulations, perhaps es (genetic drift and natural PLoS Biol. 3: 1159-1166. same can apply to the syn- in fact more often than can selection) or abruptly through Chapman MA, Burke JM (2007) thetic theory. As indicated by mutation and selection operat- hybridization, endosymbiosis, and hybrid Ryan (2006), endosymbiosis ing on already resident genes. and changes in gene regula- speciation. Evolution 61: 1773- does not contradict Darwin- Unlike eukaryotic speciation, tion. The environment plays 1780. ism, although it differs from bacterial speciation might be an important role in the evo- Coyne JA (2009) Evolution’s chal- the mutation plus-selection driven by a high rate of hori- lution of organisms, through lenge to genetics. Nature 457: paradigm of the synthetic the- zontal transfer, which intro- epigenesis. Current knowledge 382-383. ory in several respects. Natu- duces novel genes, confers allows for the rejection of the Crews D, Gore AC, Hsu TS, Dan- gleben NL, Spinetta M, Schal- ral selection does not create beneficial phenotypic capabili- central dogma of biology. Al- lert T, Anway MD, Skinner the symbiosis de novo, but ties, and permits the rapid though it seems that the study MK (2007) Transgenerational instead edits the partnership exploitation of competitive of macroevolution is not an epigenetic imprints on mate once it has become estab- environments (Doolittle, extrapolation and magnifica- preference. Proc. Nat. Acad. lished. Selection operates at 1999). tion of the events that occur Sc. USA 104: 5942-5946. the level of the partnership, Although their role in plant within populations and spe- Darwin C (1859) The Origen of Species. Peckhman M (Ed., rather than at the individual and animal evolutionary his- cies, these events cannot be 2006) Pennsylvania University level. tory remains largely unex- decoupled, since the popula- Press. Philadelphia, PA, USA. plored, suspected HGT events tion in which macroevolution 816 pp. g) have recently been identified occurs is the same population Dawkins R (1996) The Blind Watch- by Richards et al. (2009) by that evolves at the microevo- maker. Norton. New York, NY, Horizontal (or lateral) gene comparing the genome of six lutionary level. USA. 358 pp. transfer (HGT) overlaps with plant species with those of Evolutionary innovations do Doolittle WF (1999) Lateral genom- the endosymbiotic theory of 159 prokaryotic and eukary- not seem to arise at random; ics. Trends Genet. 15: M5-M8. . Endosymbiosis ba- otic species. Through phylo- on the contrary, they seem to Earl DJ, Deem W (2004) Evolvabil- ity is a selectable trait. Proc. sically involves the fusion of genetic analyses, these re- have originated from non-ran- Nat. Acad. Sc. USA 101: 11531- the entire genomes of two or- searchers found five fungi-to- dom processes based on the 11536. ganisms. Syvaven (1994) con- plant, and four plant-to-fungi epigenetic system. As a conse- Eldredge N, Gould SJ (1972) Punc- sidered this to be one part of transfers. Two of the fungi-to- quence of these developments, tuated equilibria: an alternative the larger phenomenon of plant transfers have added especially that of epigenetic to . In cross species gene transfer, phenotypes important for life inheritance, a new and wider Schopf TJM (Ed.) Models in . Freeman, Cooper which involves, in addition to in a soil environment. These definition of evolution seems & Co. San Francisco, CA, endosymbiotic fusion, the in- important results support the necessary, one that would be USA. pp 82-115. sertion of smaller genetic re- ideas of Doolittle (1999). the result of several mecha- Ekstrom TJ (1994) Parental imprint- gions, including single genes nisms that change both the ing and the IGF2 gene. Horm. or even parts of genes. The Conclusions genetic and epigenetic compo- Res. 42: 176-181. mechanisms of transfer will sitions of populations. Gilchrist GW, Lee CM (2007) All likely involve viruses, direct Though widely accepted as The integration of evo-devo stressed out and nowhere to go: transformation, conjugation, or the official scientific explana- does evolvability limit adapta- with the synthetic theory tion in invasive species? Ge- other as yet unexplored means. tion for evolution, exerting seems difficult or impossible. netica 129: 127-132. HGT (and endosymbiosis) is great influence on both our The synthetic theory is based Gould SJ (1980) Is a new and gen- an important evolutionary interpretation of biodiversity mainly on population dynam- eral theory of evolution emerg- phenomenon in the ancestry and our understanding of the ics, on the correlation of phe- ing? Paleobiology 6: 119-130. of many microbes. Doolittle world, modern synthesis lacks notypic variation with statisti- Gould SJ (1982) and the (1999) indicated that an evolu- some major elements, to wit: cal gene frequencies in popu- expansion of evolutionary theo- tionary model in which novel endosymbiosis, reticulate evo- lations, whereas evo-devo ex- ry. Science 216: 380-387. genes transferred between lution, the modern synthesis plains phenotypic change Gould SJ (2002) The Structure of Evolutionary Theory. Belknap populations play a major role of embryonic development through alterations in develop- Press. Cambrige, MA, USA. in adaptation, is radically dif- and evolution (evo-devo), epi- mental mechanisms, whether 1433 pp. ferent from one in which ad- genesis, phenotypic plasticity, they are adaptive or not. Grant R (2010) Should evolutionary aptation is achieved by selec- evolvability; which involve As a final conclusion, we theory evolve? Scientist 24: 24-25.

NOV 2010, VOL. 35 Nº 11 867 Grant-Downton RT, Dickinson HG evolution: an expanded synthe- The acquisition of new ge- based on modern evolutionary (2005) Epigenetics and its im- sis. Naturwissenschften 91: netic variation. Interciencia biology. Part 2: Retroviral sym- plications for plant biology. 1. 255-276. 33: 935-940. biosis. J. Roy. Soc. Med. 102: The epigenetic network in Lake JA (2009) Evidence for an Pigliucci M (2007) Do we need an 324-331. plants. Ann. Bot. 96: 1143-1164. early prokaryotic endosymbio- extended evolutionary synthe- Ryan JF, Mazza ME, Pang K, Ma- Grant-Downton RT, Dickinson HG sis. Nature 460: 967-971. sis? Evolution 61: 2743-2749. tus DQ, Baxevanis AD, Mar- (2006) Epigenetics and its im- Linder CR, Moret BME, Nakhleh Pigliucci M (2008) Is evolvability tindale MQ, Finnerty JR (2007) plications for plant biology. 2. LN, Warnow T (2003) Network evolvable? Nat. Rev. Genet. 9: Pre-Bilaterian Origins of the The “epigenetic epiphany”, Epi- reticulate evolution. Biology, 75-82. Hox Cluster and the Hox Code: genetics, evolution and beyond. Evidence from the Sea Anemo- models and algorithms. www. Ramsey J, Schemske DW (2002) Ann. Bot. 97: 11-27. cs.utexas.edu/phylo/resorucer. ne, Nematostella vectensis. Neopolyploidy in flowering PLoS ONE 2: e153. Ho MW (2009) How development pdf/papers plants. Annu. Rev. Ecol. Syst. directs evolution. Lecture in the Mallet J (2007) Hybrid speciation. 33: 589-639. Stebbins GL (1950) Variation and Conference Evolution and the Nature 446: 279-283. Evolution in Plants. Columbia Future. Belgrade, Serbia, 14-18 Ran L, Larsson J, Vigil-Stenman T, University Press. New York, Margulis L (1970) Origin of Eu- October 2009. Available at Nylander JAA, Ininbergs K, NY, USA. 561 pp. www.i-sis.org.uk. karyotic Cells. Yale University Zheng W-W, Lapidus A, Lowry Press. New Haven, CT, USA. S, Hasselkorn R, Bergman B Stebbins GL, Ayala F (1981) Is a Hoekstra HE, Coyne JA (2008) The 371 pp. (2010) Genome erosion in a new evolutionary synthesis nec- locus of evolution: Evo Devo Margulis L (1981) Symbiosis in Cell nitrogen-fixing vertically trans- essary? Science 213: 967-971. and the genetics of adaptation. mitted endosymbiotic multicel- Evolution 61: 995-1016. Evolution. Freeman. San Fran- Stern DL (2000) Perspective: Evolu- cisco, CA, USA. 419 pp. lular Cyanobacterium. PLoS tionary developmental biology Hotopp JCD, Clark ME, Oliveira Mayr E (1963) Animal Species and ONE 5: e11486. and the problem of variation. DCSG, Foster JM, Fisher P, Reiseberg LH (1997) Hybrid origens Evolution 54: 1079-1091 Muñoz Torres MC, Giebel JD, Evolution. Belknap Press. Cam- bridge, MA, USA. 797 pp. of plant species. Annu. Rev. Syvaven M (1994) Horizontal gene Kumar K, Ishmael N, Wang S, Ecol. Syst. 28: 359-389. Ingram J, Nene RV, Shepard J, Mayr E (2001) What Evolution Is. transfer: Evidence and possible Tomkins J, Richards S, Spiro Basic Books. New York, NY, Richards TA, Soanes DM, Foster consequences. Annu. Rev. Gen- DJ, Ghedin E, Slatko BE, USA. 336 pp. PG, Leonard G, Thomton CR, et. 28: 237-261. Tettelin H, Werren JH (2007) Mayr E (2004) 80 years of watching Talbot NJ (2009) Phylogenom- Walker EL, Panavas T (2001) Struc- Widespread lateral gene trans- the evolutionary scenery. Sci- ic analysis demonstrates a pat- tural features and methylation fer from intracellular bacteria ence 305: 46-47. tern of rare and ancient hori- patterns associated with para- zontal gene transfer between to multicellular eukaryoyes. Müller GB (2007) Evo-devo: ex- mutation and the r1 locus of Science 317: 1753-1756. plants and fungi. Plant Cell. Zea mays. Genetics 159: 1201- tending the evolutionary syn- 21: 1897-1911. Kardong KV (2003) Epigenomics: thesis. Nat. Rev. Genet. 8: 943- 1215. The new science of functional 949. Roossinck ML (2005) Symbiosis Wray GA (2007) The evolutionary versus competition in plant vi- and evolutionary morphology. Nussey DH, Postma E, Glenapp P, significance of cis-regulatory Anim. Biol. 53: 225-243. rus evolution. Nat. Rev. Micro- mutations. Nat. Rev. Genet. 8: Visser ME (2005) Selection on biol. 3: 917-924. Kimura, M (1983) The Neutral The- heritable phenotypic plasticity 206-216. ory of . in a wild bird population. Ryan FP (2006) Genomic creativity Wren JD, Roossinck MJ, Nelson Cambridge University Press, Science 310: 304-306. and natural selection: a modern RS, Scheets K, Palmer MW, synthesis. Biol. J. Linn. Soc. Cambridge, MA. USA. 367 pp. Pérez JE, Nirchio M, Alfonsi C, Melcher U (2006) Plant virus 88: 655-672. King JL, Jukes TH (1969) Non- Muñoz C (2006) Biological in- biodiversity and ecology. Plos Darwinian evolution. Science vasions. The genetic adaptation Ryan FP (2007) Virus as symbionts. Biol. 4: e80. 164: 788-798. paradox. Biol. Inv. 8:1115-1121. Symbiosis 44: 11-21. Zimmer C (2009) On the origen Kutschera U, Niklas KJ (2004) The Pérez JE, Alfonsi C, Nirchio M, Ryan FP (2009) An alternative ap- of eukaryotes. Science 325: modern theory of biological Salazar S (2008) Bioinvaders: proach to medical genetics 666-668.

868 NOV 2010, VOL. 35 Nº 11