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. Weiss).

PAM (protospacer adjacent motif, Box 1) acts with. The way this pre-selection is http://dx.doi.org/10.1016/j.tree.2015.08.003

and being incorporated into a CRISPR performed is itself subject to standard

References

locus, ‘betraying’ its original host, which Darwinian evolution of the cas (CRISPR-

1. Burkhardt, R.W. (2013) Lamarck, evolution, and the inheri-

might be doomed for extinction. It can associated) genes (Box 1). It would thus tance of acquired characters. Genetics 194, 793–805

prosper in the new host being selected be more accurate to talk about more or 2. Koonin, E.V. (2014) Calorie restriction à Lamarck. Cell 158,

237–238

for on the basis of new phenotype it less ‘deterministic’ mutagenesis [12]

3. Koonin, E.V. (2012) Does the central dogma still stand?

‘ ’ ‘ ’

acquired in the new genetic context. rather than adaptive and Lamarckian . Biol. Direct 7, 27

4. Koonin, E.V. and Wolf, Y.I. (2009) Is evolution Darwinian or/

and Lamarckian? Biol. Direct 4, 42

The second point, namely that mutations Concluding Remarks

5. Haerter, J.O. and Sneppen, K. (2012) Spatial structure and

in the CRISPR locus are adaptive, is an Scientists are obliged to describe natural Lamarckian adaptation explain extreme genetic diversity at

CRISPR locus. MBio 3, e00126–e212

illusion. First, spacers originate from ele- phenomena as accurately as possible. It is

6. Barrangou, R. and Marraffini, L.A. (2014) CRISPR-cas sys-

ments with certain signature properties, dangerous to put CRISPR in the context

tems: prokaryotes upgrade to adaptive immunity. Mol. Cell

–

such as PAM, no matter whether they of Lamarckism and adaptive mutation 54, 234 244

7. Cooper, E.L. and Overstreet, N. (2014) Diversity, evolution,

present a threat to the cell. Indeed, a because it immediately brings to mind

and therapeutic applications of small RNAs in prokaryotic

‘ ’

plasmid can carry a valuable gene and still the invisible power of life , and thus invites and eukaryotic immune systems. Phys. Life Rev. 11,

113–134

be destroyed by CRISPR. Second, it has misunderstanding. One of the main ideas

8. Hacker, J. and Carniel, E. (2001) Ecological fitness, geno-

been shown that 18% of CRISPR-harbor- that derive from Darwinism – and, in my

mic islands and bacterial pathogenicity. A Darwinian view of

–

ing organisms possess at least one view, one of the most powerful ideas in the the evolution of microbes. EMBO Rep. 2, 376 381

Trends in Ecology & Evolution, October 2015, Vol. 30, No. 10 567

9. Stern, A. et al. (2010) Self-targeting by CRISPR: gene

for these theories with data from nature is and the theories of adaptation and

regulation or autoimmunity? Trends Genet. 26, 335–340

often less than satisfactory, not least diversification.

10. Vercoe, R.B. et al. (2013) Cytotoxic chromosomal targeting

by CRISPR/Cas systems can reshape bacterial genomes

because the evolutionary processes that

and expel or remodel pathogenicity islands. PLoS Genet. 9,

e1003454 shaped a taxon usually have to be inferred Although the evidence reviewed in the

11. Grissa, I. et al. (2007) The CRISPRdb database and tools to from a single snapshot of its evolutionary book is limited to microbial experiments,

display CRISPRs and to generate dictionaries of spacers

history. Enter experimental evolution, Kassen's explicit motivation is to under-

and repeats. BMC Bioinformatics 8, 172

which permits direct replicated tests of stand the nature of biodiversity beyond

12. Koonin, E.V. and Wolf, Y.I. (2012) Evolution of microbes and

viruses: a paradigm shift in evolutionary biology? Front. Cell.

predictions under controlled conditions laboratory and beyond microbes. Jacques

Infect. Microbiol. 2, 119

[1]. Rees Kassen's Experimental Evolution Monod famously stated that what is true for

and the Nature of Biodiversity testifies to Escherichia coli is true for an elephant;

the power of experimental evolution in ironically, his discovery of operons as a

microbial systems to address such ques- major feature of bacterial genome organi-

tions and foster the development of a zation turned out not to extrapolate to

Book Review

general theory of evolutionary adaptation eukaryotes. Despite carefully discussing

Can Test-Tube and diversification. limitations and caveats, Kassen might also

be too optimistic about the extent to which

Evolution Explain

The book is structured by theory. Succes- the results from microbial experimental

Biodiversity? sive chapters introduce briefly the evolution can be extrapolated to sexual

1, assumptions, logic, and predictions con- multicellular organisms. First, he espouses

Tadeusz J. Kawecki *

cerning different aspects of adaptation the view that speciation in ‘macrobes’ is

and diversification. Kassen does an excel- usually initiated by ecologically driven diver-

lent job introducing the theory at an intui- sifying selection; he plays down the cohe-

tive level. This comes at a cost; the theory sive force of sexual reproduction, implying

is often simplified, the diversity of assump- that reproductive isolation evolves almost

tions and predictions are glossed over, as a necessary consequence of the diver-

and only a few and not always the most sifying selection. While such ‘ecological

relevant theory papers are cited. However, speciation’ does seem to occur [3], the jury

a real strength of the book is the thorough is still out as to its importance in generating

review of relevant results from microbial biodiversity of plants and animals. The

experimental evolution, summarized in alternative view is that reproductive isola-

extensive tables and correlation plots. tion in multicellular sexuals usually arises

Although the book stops short of formal through accumulation of genetic incompat-

meta-analysis, the evidence gathered pro- ibilities or through divergence of mate rec-

vides a rather convincing support for some ognition systems by sexual selection,

predictions; for example, that the rate with independently of ecological adaptation

which successive alleles are substituted [4,5]. Thus, ecological diversification may

during adaptation to a novel environment be a consequence rather than the cause of

decreases with time, or that diversification speciation. The data reviewed in Experi-

is hindered by the presence of competitors. mental Evolution and the Nature of Biodi-

Questions that need more data to be versity cannot throw much light on this

resolved are clearly identified. The focus controversy, and even microbes that

fi

What is the distribution of the tness on general models of adaptation leaves engage in occasional sex (e.g., yeast or

effects of alleles mediating adaptation to out some more specific topics, such as Chlamydomonas) are not an ideal model

a novel environment? How is the evolution the evolution of parasite virulence, on which system because they lack the extreme

of niche breadth affected by environmen- there is both rich theoretical work and a asymmetry in gamete size (or investment

tal variability? How important are antago- substantial body of data from microbial in offspring) that is the main driver of sexual

nistic pleiotropy and epistasis in evolution experiments [2]. However, within selection in plants and animals [6]. Second,

fi

diversi cation of lineages? How are rates its defined scope, Experimental Evolution I am not convinced that the predominance

fi

of diversi cation affected by ecological and the Nature of Biodiversity is not only of protein sequence over cis-regulatory

fi

interactions? Scienti c literature is replete an authoritative review of the evidence, changes in microbial evolution experiments

with theories addressing these fundamen- but also a great introduction for nonspe- helps to resolve the controversy about their

tal questions. However, empirical support cialists to both experimental evolution relative contribution to diversification of

568 Trends in Ecology & Evolution, October 2015, Vol. 30, No. 10