The role of ecology in speciation: Dolph Schluter Crafoord Laureate 2023

The Crafoord Prize is awarded in partnership between the Royal Swedish Academy of Sciences and the Crafoord Foundation in Lund. The Academy is responsible for selecting the Crafoord Laureates.

This year, the Crafoord Prize in Biosciences is awarded to the Canadian evolutionary biologist Dolph Schluter (Fig. 1) for fundamental contributions to the understanding of adaptive radiation and ecological speciation. Schluter now joins the line of prominent earlier Crafoord Laureates in Biosciences, which includes, for example, Edward O. Wilson, William Hamilton, Robert May, John Maynard Smith, Ernst Mayr, George Williams, Robert Trivers, Ilkka Hanski, Tomoko Ohta, Richard Lewontin and, most recently (2019), Sallie Chisholm.

Fig. 1.

Dolph Schluter (University of British Columbia) is the Crafoord Laureate in Biosciences 2023. Photo: Paul Joseph

Adaptive radiation refers to a concept originally developed by Simpson (1953) and is defined as ‘the evolution of ecological and phenotypic diversity within a rapidly multiplying lineage’ (Schluter 2000, p. 10). Darwin’s finches, African cichlid fish, and Hawaiian silverswords are well-known examples of adaptive radiation. Ecological speciation, which is the main mechanism behind adaptive radiation, refers to when divergent natural selection in contrasting environments leads to the evolution of reproductive isolation (Schluter 2001).

The underlying idea behind ecological speciation goes back to Darwin (1859), and it is implicit in the concept of ‘ecotypes’ developed by Turesson (1922). Furthermore, it was discussed by several of the founders of ‘the modern synthesis’ during the 1930s and 1940s (e.g. Dobzhansky 1937; Huxley 1942; Mayr 1942). The state-of-the-art of this topic at that time can be illustrated by a quote from Huxley (1942, p. 284). After having reviewed many tentative examples of how ecological divergence is associated with speciation, Huxley concluded: “Examples of this sort could be multiplied almost indefinitely. They show how widespread is the tendency to (ecological) differentiation (…) At the same time they are a challenge to biologists, since the method by which such differentiation originates is by no means clear”.

In Darwin’s view, the same process that over time changed populations also ultimately resulted in the formation of new species. Although it is sometimes said that Darwin, in On the Origin of Species, did not answer the question posed by the title of the book, this interpretation is surely wrong. As suggested by Mallet (2008), this erroneous interpretation is probably due to Darwin’s quite vague use of the species concept. After the establishment of the biological species concept based on reproductive isolation as the key feature distinguishing species (Mayr 1942), the dominant understanding became that geographic isolation (allopatry) was necessary for driving the genetic changes behind reproductive isolation. Geographic isolation per se was thus seen as the initial step in speciation, rather than divergent selection in contrasting environments, which may take place either in sympatry (when populations coexist) or in allopatry.

This situation began to change during the 1990s, and Dolph Schluter, more than anyone, made outstanding contributions of groundbreaking research exploring ecological speciation and its role in adaptive radiation. This was initially inspired by the pioneering work by Peter and Rosemary Grant on the Darwin finches on Galapagos. Indeed, Dolph Schluter's first important achievement was using the finches to study how populations of different species coexist and how this leads to divergent selection on traits to limit competition. Character displacement was a controversial idea before Schluter convincingly showed that while competing for the same resources the species of finches were more different in traits than when living alone on other islands (Schluter et al. 1985).

One other early and most influential study was the discovery of repeated evolution of new species through what he and his colleague coined ‘parallel speciation’ (Schluter and Nagel 1995). Just like in a replicated experiment, the expectation of natural selection is that divergence into different ecotypes and later species will occur again and again, under similar environmental conditions. The ultimate test of the role of natural selection is that while local barriers to gene flow have formed between the new species in each location, individuals of the same phenotype (adapted to the same type of environment) are still reproductively compatible despite being less closely related by ancestry. Exactly this evolutionary scenario, Schluter showed, was what happened in a small marine fish, the three-spined stickleback. This fish had repeatedly colonized freshwater streams and lakes and evolved similar types of adaptations in their new habitat, including the evolution of a benthic and a limnetic freshwater ecotype (Schluter and Nagel 1995). Over the years, Schluter and his colleagues have contributed numerous field studies, and in addition performed elegant manipulative experiments in specially made stickleback ponds. These studies have provided detailed knowledge about the role of selection, and how phenotypic changes link to underlying genetic changes (e.g. Peichel et al. 2001; Colosimo et al. 2005). Schluter has also highlighted the role of the standing genetic variation in evolution and how this allows rapid changes to happen even within species with relatively slow generation turn-over (Barrett and Schluter 2010). The standing genetic variation can also be redistributed through what Schluter named the ‘transporter hypothesis’ (Schluter and Conte 2009).

The results of Schluter's studies have strong relevance to one of our time's most urgent biological questions: How will the changing climate impact on the biodiversity on Earth? Are species and populations able to adapt under climate change, and under what circumstances? That rapid evolution of new adaptations can take place from standing genetic variation is encouraging, but also highlights the importance of protecting all genetic variation that is currently present in adaptive traits, since waiting for new such variation to appear will need extensively long waiting time in species (except in microbes where mutations will generate new genetic variation quite rapidly). Furthermore, the transporter hypothesis emphasizes the importance of connectivity among populations to spread useful genetic variants to new areas. Assessing the genetic variation available as standing variation is thus a very useful tool for managers of both wild and domestic species that will have to adapt to new climate regimes.

On top of the many primary contributions, Schluter has written several highly influential reviews and syntheses. For example, an early review on character displacement (Schluter and McPhail 1993), and a later synthesis paper on the role of ecology in speciation (Schluter 2001) are both seminal contributions, and in a Science review he convincingly argued that Darwin was completely correct in his conclusion that natural selection is the main driver of speciation (Schluter 2009). His outstanding book The Ecology of Adaptive Radiation (Schluter 2000) is the standard reference on the topic of ecological speciation, adding to the list of Schluter’s publications that remain having a strong impact on modern evolutionary biology. Much thanks to Dolph Schluter's work over the past 40 years, it is beyond any doubt that ecological speciation has become an established field of research (e.g. Schluter 2001, 2009; Nosil et al. 2009; Nosil 2012), forming a new research agenda and putting natural selection back in the spotlight for investigations on biological speciation.

Biographies

Kerstin Johannesson

is Professor in Marine Ecology and Member of the Royal Swedish Academy of Sciences.

Ove Eriksson

is Professor in Plant Ecology, Member of the Royal Swedish Academy of Sciences, and Chairman of the Crafoord Prize Committee in Biosciences.