A response to Michael Ruse\u27s  Bare-Knuckle Fighting: EvoDevo Versus Natural Selection 

Gilbert, Scott F.

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Swarthmore College Works Biology Faculty Works Biology 2007 Second To The Right, Straight On 'Til Morning Scott F. Gilbert Swarthmore College, sgilber1@swarthmore.edu This work is brought to you for free and open access by . It has been accepted for inclusion in Biology Faculty Works by an authorized administrator of Works. For more information, please contact myworks@swarthmore.edu. Follow this and additional works at: https://works.swarthmore.edu/fac-biology  Part of the Biology Commons Let us know how access to these works benefits you  Recommended Citation Scott F. Gilbert. (2007). "Second To The Right, Straight On 'Til Morning". Biological Theory. Volume 2, Issue 1. 74-75. https://works.swarthmore.edu/fac-biology/233 DiscussionMichael Ruse—Bare-Knuckle Fighting: EvoDevo ver-sus Natural Selection (Biological Theory 1: 402–403,2006)Second to the Right, Straight on till MorningScott F. GilbertEdward Martin Research LaboratoriesSwarthmore College, PA, USASgilber1@swarthmore.eduI thank Michael Ruse (2007) for his follow-up letter on evo-lution, selection, and development. This helps greatly in less-ening the area of perceived differences between us. Of course,seeing one’s ideas referred to in print as “hogwash” (Ruse2006) is likely to get one “riled up.”While I do confess to a tree-of-life metaphor wherein the majority of the trunk, branchesand buds are the products of development (as they are in thecorporeal tree) and where natural selection is primarily thepruner and shaper of the tree, I have no desire to see the role ofselection taken over by developmental biology. Natural selec-tionworks. It selects from the variants those that are themost ﬁtfor the environment and is critical for the origin and especiallythe maintenance of biodiversity. What I did say was that de-velopmental biology (and especially developmental genetics)is also critical for the origin and maintenance of biodiversityand deserves at least as much a place in evolutionary theoryas population genetics. In the origin of selectable variation,development should be the predominant mode of explanation.In the maintenance of variation, natural selection should dom-inate the discussions. However, both are needed.1 Moreover,because of the substantial role of development in the origin ofvariations, I also predicted (Gilbert et al. 1996) that popula-tion genetics was going to have to change its foci, if it were toremain relevant to studying important areas of evolution.Recent studies are conﬁrming this contention. As MaryJane West-Eberhard (2005: 6549) wrote in her appreciation ofErnst Mayr, “Lack of attention to developmental phenomenain relation to speciation promises to change, because genomicstudies of speciation can now contemplate gene expression aswell as gene frequency data.” This change is being seen inresearch investigating speciation in sticklebacks (reviewed inFoster and Baker 2004) and Drosophila (Michalak and Noor2003), but the new ﬁndings concerning primate evolution areprobably the most relevant. By comparing genomic regionsbetween humans and chimps, the fastest diverging areas arenot found in protein-coding sequences, but in the “darkmatter”of the genome that can regulate the expression of such genes.(This patternwas predicted2 byMary-Claire King andAllan C.Wilson in 1975, one of the papers that prompted the approachesmentioned in the Gilbert et al. article of 1996.) Speciﬁcally,several “human accelerated regions” distinguishing humanfrom chimp appear to consist of DNA elements near the genesexpressed in developing cortical neurons (Pollard et al. 2006;Prabhakar et al. 2006; reviewed by Pointing and Lunter 2006).This variation is not in the alleles normally studied by popula-tion geneticists. Nor is it in the alleles encoding developmentalregulatory proteins that have roles in forming embryonic or-gans (such as FOXP2, which is involved in speech production,or ASPM, which is involved in brain growth). Rather, this vari-ation is at yet another level—in the alleles of regulatory regionscontrolling the synthesis of developmental proteins. TheseDNA sequences determine the amount, location, and durationof developmental gene expression and may contain enhancersor encode regulatory RNAs. If these are indeed the importantloci for species differences, the traditional focus of populationgenetics is very likely to change. The comparative genomicsof developmental regulation may be able to tell us what ac-tually happened in speciation. So, I will stand by my originalcontention.The continental biologists of the late 19th century, whotried to combine embryology and Darwinism, failed. Theyfailed for several reasons—their lack of a criterion for ho-mology, the inﬂuence of Romantic Naturphilosophie, and theadherence to a notion of the Great Chain of Being, amongthem. While many of their ideas were ﬂawed (as were manyof the genetic ideas proposed after them), these embryologistsdid have some proposals that were very good; among theseJanuary 8, 2007; accepted January 9, 200774 Biological Theory 2(1) 2007, 74–75. c© 2007 Konrad Lorenz Institute for Evolution and Cognition ResearchDiscussionwas the notion that evolution consists of inherited changes indevelopment. This allowed them to look beyond the specieslevel and into the more profound levels of phylogeny, not onlyat the twigs, but at the trunks and branches of the evolutionarytree. I think that to investigate how alterations of developmentcan cause speciation as well as the major anatomical changesassociatedwith classes and phyla, we need a “deep” populationgenetics, one based on the expression of developmental genes.The combination of comparative genomics and developmentalgenetics may be presenting evolutionary biology with exactlythis type of genetics.To be called Peter Pan at age 57 is sheer ﬂattery; but Ihope that I am pointing not to an imaginary Neverland, but tothe deep time of our own planet.Notes1. Because it favors the buffering of environmental effects in some circum-stances, selection can enable the accumulation of unexpressed variation, en-abling systematic phenotypic change to occur rather suddenly. But, this ac-complishment can also be seen as a product of the developmental system. In-deed, I cannot resist mentioning the bon mot that evolutionary developmentalbiologist Jukka Jernvall (2006) made in his talk at the European Evolution-ary Developmental Biology Meeting in Prague. Showing the ways by whichchanging the synthesis and diffusion characteristics of paracrine factors cangenerate the dentition of the mammalian radiation, he proclaimed: “Nothingin variation makes sense except in the light of development.”2. Speciﬁcally, the King and Wilson (1975, p. 114) paper says, “The or-ganismal differences between chimpanzees and humans would then resultchieﬂy from genetic changes in a few regulatory systems, while amino acidsubstitutions in general would rarely be a key factor in major adaptive shifts.”ReferencesFoster SA, Baker JA (2004) Evolution in parallel: New insights from a classicsystem. Trends in Ecology and Evolution 19: 456–459.Gilbert SF, Opitz, JM Raff RA (1996) Resynthesizing evolutionary and de-velopmental biology. Developmental Biology 173: 357–372.Jernvall J (2006) The curious incident of the seal in the pond. Plenary ses-sion. European Society for Evolutionary Developmental BiologyMeeting,Prague, August 19.King M-C, Wilson C (1975) Evolution at two levels in humans and chim-panzees. Science 188: 107–116.Michalak P, Noor MA (2003) Genome-wide patterns of expression inDrosophila pure species and hybrid males. Molecular Biology and Evolu-tion 20: 1070–1076.Prabhakar S, Noonan JP, Pa¨a¨bo S, Rubin EM (2006) Accelerated evolution ofconserved non-coding sequences in humans. Science 314: 786.Pollard KS, Salama SR, Lambert N, Lambot M-A, Coppens S, Pedersen JS,Katzman S, King B, Onodera C, Siepel A, Kern AD, Dehay C, Igel H, AresM, Vanderhaegen P, Haussler D (2006) An RNA gene expressed duringcortical development evolved rapidly in humans. Nature 443: 167–172.Ruse M (2006) Forty years a philosopher of biology: Why Evo-Devo makesme still excited about my subject. Biological Theory 1: 35–37.Ruse M (2007) Bare-knuckle ﬁghting: EvoDevo versus natural selection.Biological Theory. Biological Theory 1: 402–403.West-Eberhard MJ (2005) Developmental plasticity and the origin of speciesdifferences. Proceedings of the National Academy of Sciences of the USA102: 6543–6549.Biological Theory 2(1) 2007 75

Second To The Right, Straight On Till Morning

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Second To The Right, Straight On \u27Til Morning

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