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Lamarckian Illusions spatial sorting. We are using the concept of The Lamarck Assumption Here I argue that these statements are spatial sorting presented by Shine et al. [7]: Darwinism has been under constant scru- false. I discuss, as an example, a phenom- ‘that on expanding range edges evolution- tiny ever since On the Origin of Species enon that has been used widely as evi- ary change can arise from differential dis- was published. The theory of evolution by dence for Lamarckian evolution, the persal rates (spatial sorting)’ and ‘the spatial natural selection, based on variation and CRISPR (clustered regularly interspaced sorting of genotypes caused by differential selection, provided a hitherto unparalleled short palindromic repeats) immune sys- dispersal, followed by random mating’. explanation of life's diversity and change, tem in prokaryotes. 1 invoking no forces other than simple bio- Division of Biological Sciences, University of Montana, Missoula, MT 59812, USA logical ones, such as heredity and Adaptive Mutations Not So 2 US Geological Survey, Northern Rocky Mountain Science mutation. Adaptive? Center, Glacier National Park, West Glacier, MT 59936, USA Modern physics views Newtonianmechan- 3 Flathead Lake Biological Station, University of Montana, Among recurrent themes in the disputes ics as an approximation that holds at low Polson, MT 59860, USA over Darwinism, Lamarckism holds a prom- speeds but fails to accurately describe inent place. Based on ideas of Darwin's physical relations between objects at *Correspondence: [email protected] (W.H. Lowe). predecessor Jean-Baptiste Lamarck, pub- speeds close to that of light. By analogy, http://dx.doi.org/10.1016/j.tree.2015.08.006 lished in Zoological Philosophy, Lamarck- regarding organisms as units of evolution is References ism offers a different view of organismal an approximation that does not hold at 1. Kovach, R.P. et al. (2014) Dispersal and selection mediate change based on an intrinsic drive towards the microbial and molecular scales, where hybridization between a native and invasive species. Proc. Biol. Sci. 282, e20142454 higher complexity – the ‘power of life’ – and a gene-centered perspective must be 2. Boyer, M.C. et al. (2008) Rainbow trout (Oncorhynchus an ability of the organism to directly respond adopted to fully explain certain events. mykiss) invasion and the spread of hybridization with native westslope cutthroat trout (Oncorhynchus clarkii lewisi). Can. J. to the environment, and pass the changed The reason is that, in prokaryotes, genetic Fish. Aquat. Sci. 65, 658–669 characters on to the next generation – the material is exchanged constantly via hori- 3. Fitzpatrick, B.M. et al. (2010) Rapid spread of invasive genes inheritance of acquired traits (IAT). zontal gene transfer (HGT), and microbial into a threatened native species. Proc. Natl. Acad. Sci. U.S.A. – 107, 3606 3610 populations can thus be viewed as a melt- 4. Hitt, N.P. et al. (2003) Spread of hybridization between native IAT was widely dismissed by geneticists of ing pot for genes and mobile portions of westslope cutthroat trout, Oncorhynchus clarki lewisi, and nonnative rainbow trout, Oncorhynchus mykiss. Can. J. Fish. the 20th century, but in recent decades genomes. This type of environment some- Aquat. Sci. 60, 1440–1451 research in the field of epigenetics has times favors selfish genetic elements that 5. Johnson, J.R. et al. (2010) Retention of low-fitness geno- shown that it does exist in some species, can spread at the expense of the rest of the types over six decades of admixture between native and introduced tiger salamanders. BMC Evol. Biol. 10, 147 and it has been dubbed ‘Lamarckian genome. After all, bacterial viruses (phages) 6. Allendorf, F.W. et al. (2004) Intercrosses and the US Endan- heredity’. Although a clear misnomer [1], are such mobile elements that travel gered Species Act: should hybridized populations be included as westslope cutthroat trout? Conserv. Biol. 18, it is not the focus of this article. between cells in specialized protein coats 1203–1213 they encode. 7. Shine, R. et al. (2011) An evolutionary process that assem- Epigenetics and other discoveries in bles phenotypes through space rather than through time. – Proc. Natl. Acad. Sci. U.S.A. 108, 5708 5711 molecular biology have led some scien- Recently, a remarkable defense mecha- tists to revive ‘Lamarckian evolution’ and nism, termed CRISPR, was discovered call for a paradigm shift in evolutionary that genomes employ to protect them- fi Forum biology. It has been claimed that selves from phages and other sel sh ‘Lamarckian evolution is reality rather than DNA (Box 1). A number of researchers myth’ [2], and that ‘the reality of full- claimed that CRISPR is a Lamarckian pro- Lamarckian Illusions fledged Lamarckian evolution...has been cess (e.g., [4–6]; [7] and subsequent dis- 1, convincingly demonstrated’ [3]. cussion), in the sense that (i) a mutation, Adam Weiss * In recent years the term ‘Lamarck- Box 1. Mechanism of CRISPR Immunity ian evolution’ has become a house- The CRISPR (clustered regularly interspaced short palindromic repeats) system is based on a composite hold name for processes that do not locus, wherein one portion encodes Cas (CRISPR-associated) proteins that execute the ‘immune’ follow classical Mendelian pattern response, and the other portion consists of repeat sequences interspaced by short stretches of phage of inheritance, and it is seen as a or plasmid origin (spacers). Upon entry of foreign DNA into the cell, it is recognized by the Cas machinery, and a short piece (protospacer) is incorporated into the CRISPR array. The whole array is then transcribed, relevant complement to Darwinism. and the CRISPR RNA is used during subsequent infections as a guide to complementary regions in phage In this article I argue that bringing DNA, thereby targeting it for destruction. To distinguish phage from chromosomal DNA during the acquisition of spacers and particularly during the interference phase, a 2–5 nt protospacer adjacent motif back Lamarck is unjustified and misleading. (PAM) must be recognized in the foreign DNA. 566 Trends in Ecology & Evolution, October 2015, Vol. 30, No. 10 acquired during the lifetime of an individual self-targeting spacer, and that 0.4% of all history of science – is that adaptation and cell, is non-random, elicited by a specific spacers are self-targeting [9]. These num- design can arise without any such guiding environmental factor (phage infection), bers probably dramatically understate the hand. This assertion remains true whether and inherited – in short, IAT; (ii) the muta- frequency of such ‘accidental’ acquisitions or not the adaptation leads to targeted tion is adaptive. because those that were toxic to the cell did mutations or other tricks that enhance not persist and could not be studied [10]. the plasticity of genes and genomes. The first point exemplifies the fallacy of Those that did survive did so only if the organism-centered evolution. In microbial (proto)spacers were mutated or upon par- Jean-Baptiste Lamarck was a great natu- populations, HGT (spacer acquisition is a tial degradation and loss of function of the ralist of his time. He was a vocal opponent form of HGT) is ubiquitous, and up to 18% entire CRISPR locus [9]. Moreover, of the immutability of species. He recog- of a genome can consist of horizontally CRISPR has been identified in less than nized that species change gradually and acquired genes [8]. Since HGT often half of prokaryotic genomes studied thus extremely slowly, and he even made a brings about new phenotype, it might far [11]. It is likely that, for the rest, the correct guess about exactly how slowly seem that IAT is widespread in prokar- acquisition of the locus was not adaptive (he thought in terms of hundreds of mil- yotes. Indeed, one could claim that any and they did better without it. Hence, there lions of years [1]). We should remember mutation is an IAT because a mutation is nothing a priori adaptive about spacer him for the good he contributed to generated by replication error cannot be acquisition – as true Lamarckian evolution science, not for things that resemble his distinguished from one that would arise would require – it only looks like that with theory only superficially. Indeed, thinking after taking up a piece of homologous the benefit of hindsight. The whole CRISPR of CRISPR and other phenomena as DNA (with one mismatch) and recombining system could evolve because it tends on Lamarckian only obscures the simple it into the chromosome. As a consequence, average to increase the fitness of its host and elegant way evolution really works. the difference between ‘non-random’ IAT organism – a signature feature of Darwinian and ‘random’ mutagenesis is fuzzy in the evolution. Acknowledgments microbial world. I am grateful to Renée Schroeder for support and As before, when CRISPR mutations are fruitful discussions, and to the Schroeder lab members Discussion of this kind is unnecessary if compared with other forms of HGT, we do Markus Dekens, and Gustav Ammerer for critically fi we assume the gene-centered viewpoint. not nd qualitative differences. HGT, too, commenting on the manuscript. This work was sup- A gene is the replicator subject to natural can be adaptive in disseminating valuable ported by the Austrian Science Fund (FWF grant SFB selection, and other genes in the genome genes such as antibiotic resistance genes. F4308) and the University of Vienna. can be considered its environment. If a The difference is quantitative (although we 1 Department of Biochemistry and Molecular Cell Biology, gene can proliferate more efficiently by do not know the actual numbers): CRISPR Max F. Perutz Laboratories, University of Vienna, Dr HGT than vertically, it will do so. One pre-selects from the pool of available Bohrgasse 9/5; 1030 Vienna, Austria can argue that, under some conditions, mutations on the basis of specific *Correspondence: [email protected], a protospacer can benefit from acquiring sequence characters in the DNA it inter- [email protected] (A.
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