Research Foci • Applied Dimensions • Speciation in Europe

A European model system in adaptive-radiation research: the whitefish in large Swiss pre-Alpine lakes: the central phenotype is widespread in rivers and along the shallow shores of lakes. The others are derived species, many of which are endemic to one or a few lakes. All species shown, except the one at the bottom, are sympatric in Lake Thun. © Ole Seehausen

Diversity of diversification
The entire range of evolutionary diversification mechanisms needs to be explored to understand the ecological, evolutionary, and environmental factors that favour, alternatively, the evolution of phenotypic plasticity in ecological traits, ecologically neutral differentiation in mating traits, the broadening of intraspecific polymorphisms by rearrangement of a population’s genetic architecture, the emergence of sexual dimorphisms, and – as just one among these several options – speciation. This begs questions about the mechanisms preventing speciation in the first four processes, and whether the fifth process, successful speciation, may entail the loss of diversity.

Signatures of speciation
The generation of differential testable hypotheses is urgently needed for empirically identifying alternative speciation modes and for moving towards the quantitative and standardized assessment – based on the joint utilization of phylogenetic, genetic, ecological, and spatial data – of the relative frequencies with which these modes occur in nature.

Species cohesion
The flipside of speciation is species cohesion. It remains to be understood how genetic, ecological, and spatial factors interact in preventing species from splitting. This question is particularly relevant for asexual species, and indeed for their definition, since traditional species concepts based on interbreeding can only be applicable to asexual species.

Speciation models for specific systems
There currently exists a gap between general speciation models and the features of specific natural systems. General models play an important role in the speciation debate by addressing the complexities of speciation dynamics that cannot be captured by verbal models. However, an intermediate approach will have to be established in the medium term, so that the specifics of individual systems can be integrated and explored with the same flexibility and thoroughness. Devising and calibrating such system-specific speciation models will only be successful if based on an open and intensive dialogue between empirical and theoretical experts.

The role of interspecific interactions
While the dominant selection pressures involved in speciation processes may often be intraspecific, many such processes will be strongly influenced by interspecific interactions. Both types of interactions may drive competitive, ecological, and adaptive speciation, and may also be responsible for the reinforcement of reproductive isolation in allopatrically initiated speciation. Ultimately, large-scale phylogenetic and biogeographical patterns can only be understood from a perspective sufficiently informed by, and embedded in, community ecology. Models of evolving communities and food webs have recently emerged to address the community dimension of speciation patterns and processes. Starting from only fundamental assumptions on the number of different resources, and possible types of ecological interactions, these models can be used to study the conditions under which different modes of speciation can be expected. Systematic comparisons of predictions based on ecologically detailed speciation models with those obtained from the neutral theory of biodiversity and biogeography will prove particularly important in this context. In the long-term, these seemingly disparate approaches will need to be integrated into a more encompassing overarching framework.

Speciation and bioinvasions
With the transport of alien species into new environments now being accelerated on a global scale – resulting in invading pioneers that occur in small numbers, are geographically isolated, and experience strong local selection pressures – the impacts of bioinvasions on speciation rates deserve to become better understood.

Hybridization and adaptive radiations
Since hybridization and adaptive radiations are not uncommonly occurring together, their interplay needs to be better understood. Both processes are associated with, and promoted by, colonization, but might also promote each other. Moreover, hybridization and gene flow between radiating populations may be critical for generating and maintaining genetic variation required for selection-driven speciation.

Genetics and genomics of speciation
Reproductive isolation is, in many modes of speciation, initially concentrated around a few genes and then spreads to encompass the whole genome. The technology is now available to describe genome-wide patterns of genetic differentiation, to identify key genes, and to ask about the relative importance of different types of genetic change in the build-up of reproductive isolation. New analytical techniques will be needed to make the most of the growing amounts of data available.

Biodiversity losses through reverse speciation
Since a large fraction of the world’s species diversity is of recent evolutionary origin, the ecological and evolutionary processes underlying biodiversity formation and loss deserve to be analyzed within a common framework. In particular, as much as environmental heterogeneity may foster the emergence of species, anthropogenic environmental homogenization may cause their demise.

Speciation in ecosystems
Currently available empirical and theoretical insights will have to be extended to understand the embedding of gradual evolution and speciation into multi-species communities and food webs, thus contributing to the prediction of evolutionarily robust patterns of ecosystem structure and functioning.

Evolutionary biogeography
Eco-genetic models of speciation dynamics are to be studied on increasingly realistic spatial landscapes, with the ultimate aim of devising the fundamentals of a new process-based approach to evolutionary biogeography, including an improved understanding of the evolutionary ecology of hybrid zones.

Macro-ecological explanations of biodiversity
The neutral theory of biodiversity and biogeography on the one hand, and speciation theories based on niche differentiation on the other, offer radically different views on how biodiversity arises and is maintained, highlighting a rift in the scientific understanding of biological diversity that needs to be reconciled.

Tropical forest as biodiversity hotspot. © Wolfgang Amri I Dreamstime.com

Biodiversity crisis and speciation
A region’s biodiversity is determined by the balance between the rate of species extinction through extirpation or speciation reversal compared with the rate at which new species arise through speciation and immigration. The role of speciation in this balance is generally ignored in biodiversity conservation efforts, based on the assumption that speciation rates are always too slow to contribute substantially. However, several empirical examples of fast speciation have now been documented, challenging this assumption. As data on species ages become progressively more available, we can begin to consider the biodiversity consequences of altered rates of speciation and speciation reversal.

Understanding biodiversity hotspots
It has often been argued that it is impossible to protect all global biodiversity, and that protective measures thus ought to be concentrated on biodiversity hotspots. Such hotspots are often identified by descriptive criteria, e.g., as areas with the highest species numbers in a particular taxonomic group. However, to protect future biodiversity it will be important to characterize hotspots in terms of the processes that generate new species in a hotspot and to understand what makes a particular environment conducive to the formation of new species.

Climate change and speciation
Paleontological and molecular studies suggest that periods of speciation alternate with periods of stasis. Rapid changes in the environment, for example climate, could be at the basis of punctuations in speciation rates. Understanding the consequences of large-scale environmental changes induced by humans is important, not only in terms of increased rates of extinction, but also in terms of the risks associated with the, often remarkably rapid, evolution of new ecotypes.

Speciation in agriculture and medicine
Theory on the evolution of resistance and virulence suggests that pathogens, parasites, and pests often specialise on a particular host species, because the costs associated with the development of virulence do not allow the simultaneous evolution of virulence on different host species. Coevolutionary arms races are thus likely to affect parasite diversity. Shifts in distribution caused by climate change may expose hosts to new parasites, and vice versa. Understanding speciation in pathogens, parasites, and pests is therefore of considerable relevance for medicine and agriculture.

Arctic charr in lake Thingvallavatn, Iceland. © Karl Gunnarsson	Meadow grasshopper from the Pyrenees. © Roger Butlin	Fire-bellied toad from Pinczów, Poland. © Jacek Szymura

Specitation in plants

• The European Populus tree (P. alba or White poplar, and P. tremula or European aspen) is becoming established as a model for research on the genetics of species barriers. Work on this genus benefits from a near-complete genome sequence and high applied interest with regard to carbon mitigation. Instead of directly dealing with the process of speciation, European Populus offers a case of ‘porous’ species boundaries resulting from secondary contact and thus allows studying the maintenance of species barriers.
• The salt marsh grass species Spartina anglica (Poaceae) is a nascent allopoly-ploid formed in England during the end of the 19th century by hybridization between an indigenous and an invasive species. It has rapidly expanded in range, and has now invaded several continents. This species has larger ecological amplitude than its parental species and illustrates particularly well the short-term success of a new species following hybridization and genome duplication.
• Orchids in the genus Ophrys attract male hymenopterans by mimicking sex pheromones and are pollinated by pseudocopulation. Coevolution between pollinaters and orchids underlies sympatric diversification in this genus, and a role for selection on floral odour in promoting differentiation has been suggested.

Specitation in fish

• Arctic charr (Salvelinus alpinus) often form eco-morphs in lakes. In many cases, these morphs are genetically distinct. Lake Galtaból in Iceland harbours eco-morphs for which the analysis of microsatellite variation strongly indicates complete reproductive isolation. This example has been referred to as one of three studies (of many candidates) strongly suggestive of sympatric speciation. In addition, some dwarf forms of Icelandic Arctic charr, living in confined cold spring habitats, may be on the road to allopatric speciation. Also two morphs of arctic charr – one littoral, the other profundal – in the Norwegian Lake Fjellfrøsvatn have been documented to exhibit reproductive isolation in space and time, segregation of their ecological niches, genetic differentiation, as well as genetically based differences in morphology and behaviour. Coexisting ecomorphs of arctic charr are known also from several Swiss lakes.
• Three-spined stickleback (Gasterosteus aculeatus) often form morphs within lakes that show clear signs of genetic, ecological, and morphological divergence. In Iceland, such divergence has occurred at a timescale of no more than 2000 generations (about 10,000 years). Stickleback is already an important model species for speciation studies in North America and has recently become a genome species, with a full genome sequence only just published (http://www.ensembl.org/Gasterosteus_aculeatus/index.html). Parallel cases of speciation in different European settings are studied by several labs.
• Whitefish (Coregonus spp) are becoming one of the major vertebrate model systems for studying rapid speciation and adaptive diversification. European centres of diversification are the pre-Alpine lake system with up to 20 parallel adaptive radiations, ranging from 2 to 7 incipient species per lake, and the Fenno-Scandian lake systems from Lake Onega in the East to Norway in the West. Smaller radiations exist in other parts of Europe, like the United Kingdom, northern Germany, and Poland. Using this system across the European distribution of the genus Coregonus thus offers unique opportunities for developing a comparative adaptive radiation research program.
• The trout, Salmo trutta, is a species complex covering all Europe. Five main geographic lineages have been described and all are interfertile, with interbreeding occurring through natural secondary contacts or human translocations. In total eight deeply differentiated forms of trout have been identified, creating examples at the frontier between species and differentiated populations.
• Recently, it has been established that the species of bullheads (Cottus gobio) in fact constitutes a species complex, with derived species of recent hybrid origin in the lower reaches of the River Rhine.
• Genesis and maintenance of the species complex of Iberian minnows, Squalius alburnoides, involves polyploidy, hybridisation, and variation in mating systems. While S. alburnoides populations are mainly composed of triploid and diploid hybrid forms, two symmetric allotetraploid populations were found to resume normal meiosis after undergoing intermediate processes of non-sexual reproduction. The resultant new sexually reproducing polyploid species in the Iberian Douro river, illustrate how hybrid polyploid complexes may lead to speciation.

Specitation in birds

• Recent analyses natural hybridization between pied flycatchers (Ficedula hypoleuca) and collared flycatchers (F. albicollis) have shown that both phenotypically plastic sexual signals (e.g., song) and genetically determined sexual signals (e.g., plumage) cause reproductive isolation between the two species.
• The crossbill (Loxia curvirostra) in North America features cryptic species feeding on different species of conifers, recognizable by vocalisations and bill morphology. In Europe, assortative mating between different vocal types has been found, and also morphological differentiation between vocal types has been documented.
• The nightingale (Luscinia megarhynchos) and the thrush nightingale (Luscinia luscinia) are morphologically and ecologically very similar species that hybridise in a narrow region of sympatry. According to Haldane’s rule, hybrid females are sterile, while hybrid males are fertile. Preliminary results show that the Z chromosome contributes disproportionately to reproductive isolation, highlighting similarities in the genetic basis of reproductive isolation in organisms with heterogametic males and females.

Specitation in snails

• Morphologically distinct forms of the periwinkle (Littorina saxatilis) have evolved independently on steep environmental gradients on the coasts of Spain, Sweden, and England, and even in geographically distant localities from Spain. These populations show varying degrees of reproductive isolation through local adaptation, habitat choice, assortative mating, and genetic incompatibility. These ecotypes show differences in morphometric, biochemical, behavioural, ecological and genetic traits being consequence of their adaptation to distinct micro-habitats.
• Morphologically and genetically distinct forms of the speciose door-snail Albinaria show varying degrees of (mostly pre-mating) reproductive isolation. A weak association with genetic divergence and environmental conditions may indicate non-adaptive radiation and a profound role for sexual selection as a driver of differentiation.

Specitation in insects

• Damselflies of the genus Calopteryx have diverged in their degree of melanistic wing colouration, a trait subject to both natural and sexual selection that also contributes to sexual isolation between species. While previous work on this genus has focused on North American species, recent years have witnessed increased contributions by European research groups. In particular, sexual isolation between parapatric populations of C. splendens have recently been demonstrated.
• A European example of host race formation in phytophagous insects is that of Ostrinia nubilalis, the European corn borer. This species is a pest of corn in both North America and Europe. However, in Europe there exists a genetically distinct population on Artemisia vulgaris, with mating preference for its own kind, likely representing a recent host shift
• Grasshoppers in the genus Chorthippus provided a classical example of the role of mating-signal divergence in reproductive isolation and was the subject of one of the first phylogeographic analysis of post-glacial colonisation involving parapatric speciation. Investigations of a hybrid zone in the Pyrenees and Alps have shown that selection following secondary contact can break down gene combinations responsible for hybrid male sterility and has yielded much information about the morphometric, biochemical, behavioural, ecological, chromosomal, genetic, and molecular genetic aspects of the underlying evolutionary processes.

Specitation in other animals

• Many species of mice (Mus spp) are now recognized in Europe. The most recent addition stems from the recent discovery of the new species Mus cyprianus on Cyprus. Analyses of hybrid zone between two subspecies of house mouse, Mus musculus musculus and Mus musculus domesticus, as well as genetic crosses have shown that X chromosome has disproportionately large effect in speciation.
• The fire-bellied toads, Bombina bombina and B. variegata, are highly dissimilar species that hybridize in a long, but narrow, zone that stretches across the European continent. Several detailed analyses along transects show that introgression is limited by selection at multiple loci. The Bombina hybrid zone offers a window on some important evolutionary processes underlying speciation, and has been at the forefront of research for the last two decades.

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Last updated: 04 Sep 2011