Parallel Speciation

by

Kerstin Johannesson

• LAST MODIFIED: 21 June 2024
• DOI: 10.1093/obo/9780199941728-0154

Introduction

Parallel speciation is a young concept, derived as a specific case from the more general concept of parallel evolution. It was coined by Dolph Schluter and Laura Nagel in a seminal paper from 1995. In this paper they illustrated parallel speciation using the three-spined stickleback that repeatedly form freshwater ecotypes from marine ancestral populations. However, already in 1993 Schluter and McPhail provided a review on “replicate adaptive radiation” discussing parallel evolution of fish ecotypes in postglacial lakes and of Anolis lizards on Caribbean islands. Parallel speciation is essentially equivalent to parallel evolution of reproductive isolation, and both can be partial rather than complete. And similar to the more general discussion on speciation, it is mostly impossible to draw the line between partial and complete. The core attribute of parallel speciation is that traits leading to reproductive isolation evolve repeatedly and independently when a species is distributed over contrasting environments. The driver of parallel speciation is divergent natural selection. Mostly the reproductive barriers are not the direct target of selection but evolve as a by-product of repeated adaptation to different environments. For example, a species evolves into a small ecotype in one type of habitat and a large in another, and due to the size differences individuals of the different ecotypes avoid mating with each other while individuals from different locations of the same ecotype remain compatible. The expectation under parallel speciation is that barriers to reproduction between different ecotypes establish in contact zones where the environment shifts, despite these populations being phylogenetically the most closely related. However, there are no barriers between individuals of similar ecotype coming from different areas (when these are brought together in experimental tests).

Parallel Evolution and Ecotypes

Parallel speciation (as coined by Schluter and Nagel 1995, and described already in Schluter and McPhail 1993) is closely related to the much older concept of “ecotypes” introduced by Göte Turesson in Turesson 1922. Turesson described varieties of plants locally adapted to different types of environments by divergent selection, although he did not explicitly consider the level of reproductive isolation that evolved between contrasting ecotypes of a species. Similar to evolution of ecotypes, parallel speciation is acknowledged as strong evidence for the role of natural selection in forming new species under ecological speciation. Empirical patterns illustrating parallel speciation can alternatively be explained by other models (see Competing Hypotheses) and these need to be rejected using, for example, demographic analysis. Parallel speciation is of course closely related to parallel evolution, and consequently, there is a relationship to convergence which is not yet fully resolved. Depending on what level of organization that is in focus (nucleotides, amino acids, genes, metabolic and signaling pathways, organismal traits), it can either be described as convergence or parallel evolution. For example, mutations on different genes may result in very similar phenotypic changes, reflecting convergence at the molecular level and parallelism at the phenotypic level. Mostly, authors discussing parallel evolution consider it at the phenotypic level, independent of the molecular background, but there are many exceptions and examples of discussions of parallelism at lower levels. Importantly, parallelism leading to parallel phenotypic changes can also be the consequence of developmental constraints. A brief description of this with some examples are presented in the textbook Stearns and Hoekstra 2005. This developmental parallelism is important to bear in mind but is unlikely to be involved in reproductive barriers and will not be further treated here. One additional case of parallel speciation is found in species of plants where the same chromosomal rearrangement can happen repeatedly, through hybridization and chromosomal duplication (or sometimes without). One such example is described by Schwarzbach and Rieseberg 2002, but these types of repeated hybrid speciation are at least partly by a completely other mechanism than the one described by Schluter and Nagel 1995 and is outside the scope of this review.

• Schluter, D., and J. D. McPhail. 1993. Character displacement and replicate adaptive radiation. Trends in Ecology and Evolution 8:197–200.

  DOI: 10.1016/0169-5347(93)90098-A

  This review was the first to describe parallel evolution of reproductive traits as “replicate adaptive radiation.” The review summarizes evidence for character displacement in following repeated radiations of fish species in postglacial lakes and of lizards on tropical islands. The authors argue that chance events can be excluded and that these examples illustrate how character displacement (by natural selection) result in morphological and ecological divergence that finally result in speciation and adaptive radiation of new species.

• Schluter, D., and L. M. Nagel. 1995. Parallel speciation by natural selection. The American Naturalist 146:292–301.

  DOI: 10.1086/285799

  Parallel speciation is defined as “the repeated independent evolution of the same reproductive isolating mechanism.” It is the consequence of parallel evolution of phenotypic divergence resulting in reproductive barriers and a special case of parallel evolution. The authors list four criteria for parallel speciation: (1) parallel traits should have evolved independently, (2) reproductive isolation should have evolved between the diverging populations, (3) no reproductive isolation should have evolved between the populations adapted to similar environments, and (4) adaptation to the local environments need be identified and the mechanism tested.

• Schwarzbach, A. E., and L. H. Rieseberg. 2002. Likely multiple origins of a diploid hybrid sunflower species. Molecular Ecology 11:1703–1715.

  DOI: 10.1046/j.1365-294X.2002.01557.x

  This paper describes repeated formation of a hybrid species (Helianthus anomalus) through cross breeding between H. annuus and H. petiolaris. This example of hybrid speciation is unusual in that instead of doubling the number of chromosomes, the new species remains diploid. Nevertheless, the results indicate that the new species was formed at least at three separate times, and that the involvement of deterministic forces seems necessary to explain the otherwise unlikely event.

• Stearns, S., and R. Hoekstra. 2005. Evolution. 2d ed. London: Oxford Univ. Press.

  A textbook that brings up the alternative mechanism causing parallel divergence. While divergent natural selection is a key mechanism in parallel evolution and parallel speciation, an alternative mechanism might be formation of parallel phenotypic traits due to developmental constrains. This is why it is important to consider the fourth criteria of Schluter and Nagel 1995.

• Turesson, G. 1922. The species and the variety as ecological units. Hereditas 3:100–113.

  DOI: 10.1111/j.1601-5223.1922.tb02727.x

  Turesson introduces the concept of “ecotype” meaning divergence of populations of a species through adaptation to different types of environments. While Turesson was unable to identify the ancestral relationships of the different populations and ecotypes, his descriptions and common garden experiments clearly showed he was dealing with phenotypic parallelism. Today, the ecotype concept has gained renewed interest and reproductive isolation between ecotypes of a species is a main focus for research on parallel speciation.