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3 Hulme, P.E. (2011) Addressing the threat to biodiversity from botanic gardens. Trends Ecol. Evol. 26, 168174 4 McCracken, D. (1997) Gardens of Empire: Botanical Institutions of the Victorian British Empire, Leicester University Press 5 Aikio, S. et al. (2010) Time lags in alien plant invasions: separating the facts from the artefacts. Oikos 119, 370378 6 Davis, K. (2008) A CBD Manual for Botanic Gardens, Botanic Gardens Conservation International 7 Hulme, P.E. and Weser, C. (2011) Mixed messages from multiple information sources on invasive species: a case of too much of a good thing? Divers. Distrib. DOI: 10.1111/j.1472-4642.2011.00800.x

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8 Dawson, W. et al. (2009) The suitability of weed risk assessment as a conservation tool to identify invasive plant threats in East African rainforests. Biol. Conserv. 142, 10181024 9 Virtue, J.G. et al. (2008) Australias botanic gardens weed risk assessment procedure. Plant Prot. Q. 23, 166178 10 Jefferson, L. et al. (2004) Implementing invasive screening procedures: the Chicago Botanic Garden model. Weed Technol. 18, 14341440
0169-5347/$ see front matter 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2011.06.005 Trends in Ecology and Evolution, September 2011, Vol. 26, No. 9

Letters

When are genes leaders or followers in evolution?

Tobias Uller1 and Heikki Helantera 2
1 2

Edward Grey Institute, Department of Zoology, University of Oxford, OX1 3PS, UK Department of Biosciences, University of Helsinki, POB 65, FI-00014, Finland

In a recent inspiring review, Schwander and Leimar (S&L; [1]) make a case for how comparative studies of polymorphisms can contribute to a synthesis of developmental and evolutionary biology. In particular, they set out to test whether genes are leaders or followers in evolution [2]. Although we endorse S&Ls intentions, we believe their approach to be of limited utility for assessing whether adaptive phenotypic change originates with environmental induction followed by genetic accommodation or, as the standard view of evolution would have it, with novel genetic variation alone. Environmental induction of novel phenotypes can form the rst step in evolutionary change because environmentally induced phenotypes with different genotypes can be recurrent in the context in which they are selected. This facilitates secondary adjustment of the regulation or form of phenotypes via natural selection on genetic variation, a process referred to as genetic accommodation [2]. In contrast to the modern synthesis framework of evolution, most gene frequency change under this scenario is a consequence, rather than a cause, of the origin of adaptive traits. In the most comprehensive treatment of this topic to date, Mary-Jane West-Eberhard referred to this as a scenario where genes are followers, rather than leaders, in adaptive evolution [2], a terminology adopted by S&L. It seems to us that S&Ls approach is unable to address this hypothesis. Firstly, alternative phenotypes are only determined by a single genetic or environmental input in the sense that those inputs are decisive for the expression of a particular morph under extant species-typical circumstances. This derived situation does not necessarily explain how those phenotypes originated. For example, we can plausibly envision a scenario where a genetically determined polymorphism is suggested by phylogenetic reconstruction to be the ancestral state, even if alternative phenotypes evolved via environmental induction followed by genetic accommodation of their expression, e.g. chapters 6, 20 and 26 in [2]. Thus, the developmental origin of
Corresponding author: Uller, T. (tobias.uller@zoo.ox.ac.uk).

alternative phenotypes is likely to be poorly captured by extant patterns of morph determination (see below). Secondly, assigning genes as leaders or followers in evolution based on the direction of the shift between systems of morph determination (i.e. G ! E vs E ! G inferred from the phylogenetic pattern) risks confusing the role of developmental plasticity in the origin and maintenance of alternative phenotypes with its role in the evolution of regulation of the expression of those phenotypes. For example, a single mutation may trigger an evolutionary transition from environmental (ESD) to genotypic sex determination (GSD) by causing a genetic element to lose environmental sensitivity in its expression [35]. If so, GSD may be a derived condition (genes are followers in S&Ls terminology), but genes were leaders in the evolutionary transition between modes of phenotype control (i.e. GSD evolved from ESD via selection on a novel genetic variant alone and not via environmental induction). On the contrary, the wide-spread environmental sensitivity of sex determination in species with sex chromosomes points towards the possibility that environmentally induced changes may initiate evolutionary shifts from GSD to ESD [2,3]. If so, genes may be leaders with respect to the phylogenetic pattern of morph determination (i.e. GSD is the ancestral state), but developmental plasticity would initiate the evolutionary transition (i.e. genes would be followers in the evolutionary transition to ESD). Although there are potential empirical examples of both scenarios [13], they remain to be convincingly demonstrated by data. The lack of convincing empirical examples is perhaps not surprising. Assessing the role of developmental plasticity in evolution and whether genes are leaders or followers in this sense requires studies that investigate whether the evolution of complex phenotypes is better explained by a sequence that begins with environmental induction followed by genetic accommodation or by successive bouts of selection on standing genetic variation or novel mutations alone [2,6]. This is an outstanding empirical challenge, and progress is likely to be facilitated by focusing on recent
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events where the origin and evolution of adaptive phenotypes can be studied directly [7]. Comparative studies may also provide important insights into this process if it can be established that phenotypic accommodation of novel environmental input in ancestral lineages or populations mirrors phylogenetic divergence (e.g. [811]). In conclusion, it seems to us that S&Ls notion of genes as leaders or followers in evolution is very different from that discussed in the literature on the evolutionary implications of developmental plasticity, e.g. [2,611]. We do not imply that the terminology is better suited for one or the other purpose. However, the move from treating genes as followers when environmental induction initiates evolutionary change, to treating it as a description of the phylogenetic pattern of morph determination, as in S&L, may risk confusing pattern with process. Nevertheless, Schwander and Leimar have provided researchers with a strong incentive for assessing in more detail the developmental regulation of morph expression and its sensitivity to novel input in a comparative context.
References
1 Schwander, T. and Leimar, O. (2011) Genes as leaders and followers in evolution. Trends Ecol. Evol. 26, 143151

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2 West-Eberhard, M.J. (2003) Developmental Plasticity and Evolution, Oxford University Press , H. From the origin of sex-determining factors 3 Uller, T. and Helantera to the evolution of sex-determining systems. Quart. Rev. Biol. (in press) 4 Wilkins, A.S. (2002) The Evolution of Developmental Pathways, Sinauer Assoc Inc. 5 Sarre, S.D. et al. (2004) The ends of a continuum: genetic and temperature-dependent sex determination in reptiles. Bioessays 26, 639645 6 Moczek, A.P. (2007) Developmental capacitance, genetic accommodation, and adaptive evolution. Evol. Dev. 9, 299305 7 Badyaev, A.V. (2009) Evolutionary signicance of phenotypic accommodation in novel environments: an empirical test of the Baldwin effect. Philos. Trans. R. Soc. Lond. B 364, 11251141 8 Badyaev, A.V. and Oh, K.P. (2008) Environmental induction and phenotypic retention of adaptive maternal effects. BMC Evol. Biol. 8, 3 9 Pfennig, D.W. and Martin, R.A. (2009) A maternal effect mediates rapid population divergence and character displacement in spadefoot toads. Evolution 63, 898909 10 Scoville, A.G. and Pfrender, M.E. (2010) Phenotypic plasticity facilitates recurrent rapid adaptation to introduced predators. Proc. Natl. Acad. Sci. U.S.A. 107, 42604263 11 Pfennig, D.W. et al. (2010) Phenotypic plasticitys impacts on diversication and speciation. Trends Ecol. Evol. 25, 459467
0169-5347/$ see front matter 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2011.05.013 Trends in Ecology and Evolution, September 2011, Vol. 26, No. 9

Letters Response

The evolution of novel cues for ancestral phenotypes

Tanja Schwander1 and Olof Leimar2
1

Evolutionary Genetics, Centre for Ecological and Evolutionary Studies, University of Groningen, 9700 CC Groningen, The Netherlands 2 Department of Zoology, Stockholm University, 10691 Stockholm, Sweden

Recent years have seen a growing interest in the role of developmental plasticity in evolution, with issues ranging from adaptive diversication and speciation to the evolution of novel phenotypes [1]. In a recent article in TREE, we argued that insights into the importance of plasticity can be gained by inferring transitions between environmental and genetic control of discrete alternative phenotypes [2]. Our approach can reveal whether phenotypes that currently occur as genetic polymorphisms, or as monomorphisms in different populations, were previously elements of reaction norms and, conversely, whether environmentally induced alternative phenotypes derive from genetically controlled variants. We described the two evolutionary sequences as plasticity rst and genetic polymorphism rst and also labelled them as genes as followers and genes as leaders, respectively. (U&H; [3]) criticise our approach in Uller and Helantera two ways. First, because we did not address the origin of alternative phenotypes, our approach cannot detect whether phenotypic change originates as environmental induction of novel phenotypes, followed by genetic accommodation. U&H regard this latter process as the major
Corresponding author: Schwander, T. (tanja.schwander@gmail.com); Leimar, O. (olof.leimar@zoologi.su.se).

conceptual alternative to the standard view of evolution [3]. Second, the terminology of genes as followers is only appropriate for such inductionaccommodation sequences. To judge the merits of the criticism, one should ask how helpful the pitting of inductionaccommodation sequences against all other forms of evolutionary change is for assessing the importance of plasticity in evolution. We agree that environmental induction of truly novel phenotypes, followed by genetic accommodation, is an interesting process worthy of study. Nevertheless, there are few empirical examples illustrating this process, so perhaps it has a limited role in phenotypic evolution. A broader view of the role of plasticity, that includes cases where already existing phenotypes become induced by novel environmental or genetic cues, might then be preferable. The specic examples that U&H cite in fact suggest that such a broader view is worthwhile. So, in Arizonian house nch populations, adaptive clustering of female versus male offspring along the egg-laying sequence is triggered by mite infestations [4]. Such infestations do not occur in recently colonized northern locations, but sex clustering is induced by exposure to cold temperatures [5]; therefore, the same phenotype is induced by different cues. Phenotypic divergence between spadefoot toad populations might derive from pre-existing developmental and transgenerational

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