Pilpel and Rechavi Biology Direct (2015) 10:34 DOI 10.1186/s13062-015-0062-9 COMMENT Open Access The Lamarckian chicken and the Darwinian egg Yitzhak Pilpel1* and Oded Rechavi2* Abstract: “Which came first, the Chicken or the Egg?” We suggest this question is not a paradox. The Modern Synthesis envisions speciation through genetic changes in germ cells via random mutations, an “Egg first” scenario, but perhaps epigenetic inheritance mechanisms can transmit adaptive changes initiated in the soma (“Chicken first”). Reviewers: The article was reviewed by Dr. Eugene Koonin, Dr. Itai Yanai, Dr. Laura Landweber. Keywords: Evolution, Darwinian Evolution, Lamarckian Evolution, Modern Synthesis, Weismann Barrier, Epigenetic Inheritance, Transgenerational RNA Interference Background solution. Nevertheless, it is important to discuss why this In this commentary paper we wish to use the well- question is perceived as being paradoxical, and to exam- known “Chicken and Egg” paradox as a gateway for ine the true mystery that it holds; at the base of this discussing different processes of evolution. While in the dilemma stands an extremely important and unsolved biological sense this is not a paradox at all, the metaphor biological question: “Can the phenotype affect the is still useful because it allows examining of the distinc- genotype”? or put differently, “Can epigenetics translate tion between Lamarckian and Darwinian evolution, and into genetics”? specifically, since it enables us to raise an important and Asking the question in this manner allows mapping of unsolved question: “Can the phenotype affect the geno- the “Egg first” vs. the “Chicken first” options onto the type?” or in other words, “can epigenetics translate into distinction between Darwinian and Lamarckian evolu- genetics”? tion. We wish to suggest that while in many speciation events the “Egg” indeed came first, in some cases, The only apparent paradox speciation resulted from diverse types of epigenetic inhe- “ ” The “Chicken and the Egg Question” or “Which came ritance mechanisms, and thus have a Chicken first first, the chicken or the egg?” is a well-known metaphor- origin (Fig. 1). ical paradox. The original and biologically-relevant ques- While the question is not truly paradoxical, since an “ ” “ ” tion, which has been discussed already by ancient Greek imagined Egg can precede a Chicken or vice versa philosophers (e.g. “If there has been a first man he must (because organisms are constantly evolving and new spe- have been born without father or mother – which is cies gradually emerge), we ask - which came first? Let us repugnant to nature” Aristotle), became synonymous start by defining what we mean when we use the meta- ” ” “ ” with paradoxes in general, since it presents a classical phors, Chicken and Egg . catch: when two events appear to serve both as the cause and the effect of one another it is inconceivable to grasp The chicken that any one of them could have preceded the other. There is no archetype “Chicken” which is essentially dif- While the metaphysical question might be impossible ferent from its non-chicken ancestor. Richard Dawkins to resolve, we wish to suggest here that the “Chicken called the human tendency to perceive organisms as and the Egg” question is not a paradox at all, since members of very discrete “species”,as“the tyranny of precise definition of the question and examination of the the discontinuous mind”. He stressed that all organisms possible underling mechanisms of evolution offer a exist in a continuum of evolutionary changes, and wrote “there was never a Australopithecus mother who gave * Correspondence: [email protected]; [email protected] ” “ ” 1 birth to a Homo child [4]. Thus, the new organism, Department of Molecular genetics, Weizmann Institute of Science, Rehovot “ ” 76100, Israel the Chicken , that in our story hatched from a non- 2Department of Neurobiology, Wise Faculty of Life Sciences & Sagol School, Chicken “Egg”, is still, by and large, a “Chicken”, albeit a Tel Aviv University, Tel Aviv 69978, Israel © 2015 Pilpel and Rechavi. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http:// creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Pilpel and Rechavi Biology Direct (2015) 10:34 Page 2 of 5 scenario to be considered, transgenerational inheritance of somatically acquired traits, via epigenetic processes, must take place. Thus the “Chicken first” situation in- volves evolutionary mechanisms similarly to those envi- sioned by Lamarck. Evolution according to Lamarck, as described 50 years before the publication of Darwin’s work, is driven by the inheritance of acquired cha- racteristics. According to Lamarck, organisms adapt by developing new variations in response to changing envi- ronments, and these new adaptive traits become herit- able. Because of the apparent teleological nature of his theory, since it appears to clash with Mendelian genetics, and because no mechanism that enables inheritance of acquired traits was known, Lamarck’s theory was con- sidered, for 200 years, to be completely wrong (E. V [12]). “Can epigenetics translate into genetics? For the sake of accuracy, and although certain historians consider it to be his “greatest mistake”,itisimportanttore- Fig. 1 Depending on whether evolution was purely Darwinian or member that at the late stages of his life, Darwin accepted also Lamarckian, both the Egg of the Chicken could “come first” the notion of inheritance of acquired traits [3]. Thus, the old Darwin at least, might have tolerated a “Chicken first” explanation as well. It was August Weissman who hypo- chicken which harbors certain heritable phenotypical thesized the existence of a barrier to transfer of genetic changes that distinguishes it from its ancestor. The for- information between the soma and the germline. This dis- mal, dictionary definition of a “Species”–whether tinction, in theory at least, made Lamarckism untenable or not the progeny can produce fertile offspring with [8, 22]. Also, it must be emphasized that the “Chicken or members of its parents’ specie – is irrelevant to this Egg” question as we define it here (germline Vs. soma), is discussion. valid even when all agree that Natural Selection and Drift are the primary processes by which evolution advances. The egg Responses to challenges, and epigenetic changes, which To deal with the evolutionary mechanism at the heart of could originate also in somatic cells that interact with the this apparent paradox, we wish to only consider here environment, can be selected and maintained similarly to organisms that have somatic cells and dedicated germ random mutations in the DNA ([2, 8]; E. V. [10, 13]). cells. The “Egg” in this manuscript, is a germ cell, a While classic DNA-based Mendelian genetics supports sperm or an oocyte. According to the Modern Synthesis the existence of August Weismann’s theoretical barrier only mutations that occur within the germline are inher- between the soma and the germline, and thus “Egg first” ited to next generations. solutions only, in recent years discovery and charac- terization of epigenetic mechanisms that enable trans- Where did the genetic change originally occur, in the mission of somatically acquired traits across generations Soma or in the Germline? may support “Chicken first” scenarios as well. Since this Our original “Chicken and Egg” question can now be is not an exhaustive review of the subject, we will not reframed as: did the heritable change(s) that gave rise to get into the details of the different mechanisms, but will the first Founding Individual in a given speciation event simply note that these include epigenetic mechanisms originate in the germline of its parent or in the soma of that affect the chromatin, and may or may not be segre- that individual. Or, more specifically: “Where did the gated with the chromosomes according to Mendel’s laws genetic change originate, in the soma of the hen, or of (DNA methylation, histone modifications) ([6]; Katz, the rooster, in the eggs its mother or in the sperm of its Edwards, Reinke, & Kelly, [9, 14];; Dias & Ressler 2014), father”? epigenetic mechanisms that “flirt” (interact) with the An “Egg first” solution to the so-called paradox is DNA, such as non coding RNAs-mediated gene re- certainly easy to imagine, compatible with the “Modern gulation ([1, 5, 15, 17, 18]; Rechavi, Minevich, & Hobert, Synthesis” between Darwin and Mendel, and probably [19, 21]), and DNA-independent inheritance mecha- explains many “speciation” events; in that respect the nisms (e.g. prions, protein feed back loops, hormones, Egg indeed “came first” in most cases. For the second metabolites) [7, 8]. Pilpel and Rechavi Biology Direct (2015) 10:34 Page 3 of 5 For speciation to occur as a consequence of Chicken- Is there evidence to suggest that inheritance of ac- first epigenetic responses, two barriers need to be crossed: quired traits has actually allowed “Chickens” to precede the epigenetic to genetic, and the somatic to germline. “Eggs”? How prevalent are such instances? Crossing the first barrier means that certain inherited epi- This is an exciting and very active field of research, genetic effects must