The cichlid fish radiations in the African Great Lakes differ from all other known cases of rapid speciation in vertebrates by their spectacular trophic diversity and richness of sympatric species, ...comparable to the most rapid angiosperm radiations. I review factors that may have facilitated these radiations and compare these with insights from recent work on plant radiations. Work to date suggests that it was a coincidence of ecological opportunity, intrinsic ecological versatility and genomic flexibility, rapidly evolving behavioral mate choice and large amounts of standing genetic variation that permitted these spectacular fish radiations. I propose that spatially orthogonal gradients in the fit of phenotypes to the environment facilitate speciation because they allow colonization of alternative fitness peaks during clinal speciation despite local disruptive selection. Such gradients are manifold in lakes because of the interaction of water depth as an omnipresent third spatial dimension with other fitness-relevant variables. I introduce a conceptual model of adaptive radiation that integrates these elements and discuss its applicability to, and predictions for, plant radiations.
The African cichlid fish radiations are the most diverse extant animal radiations and provide a unique system to test predictions of speciation and adaptive radiation theory. The past few years have ...seen major advances in the phylogenetics, evolutionary biogeography and ecology of cichlid fish. Most of this work has concentrated on the most diverse radiations. Unfortunately, a large number of small radiations and 'non-radiations' have been overlooked, potentially limiting the contribution of the cichlid system to our understanding of speciation and adaptive radiation. I have reviewed the literature to identify 33 intralacustrine radiations and 76 failed radiations. For as many as possible I collected information on lake size, age and phylogenetic relationships. I use these data to address two questions: (i) whether the rate of speciation and the resulting species richness are related to temporal and spatial variation in ecological opportunity and (ii) whether the likelihood of undergoing adaptive radiation is similar for different African cichlid lineages. The former is a key prediction of the ecological theory of adaptive radiation that has been presumed true but remains untested for cichlid radiations. The second is based on the hypothesis that the propensity of cichlids to radiate is due to a key evolutionary innovation shared by all African cichlids. The evidence suggests that speciation rate declines through time as niches get filled up during adaptive radiation: young radiations and early stages of old radiations are characterized by high rates of speciation, whereas at least 0.5 Myr into a radiation speciation becomes a lot less frequent. The number of species in cichlid radiations increases with lake size, supporting the prediction that species diversity increases with habitat heterogeneity, but also with opportunity for isolation by distance. Finally, the data suggest that the propensity to radiate within lakes is a derived property that evolved during the evolutionary history of some African cichlids, and the appearance of which does not coincide with the appearance of proposed key innovations in morphology and life history.
A Combinatorial View on Speciation and Adaptive Radiation Marques, David A.; Meier, Joana I.; Seehausen, Ole
Trends in ecology & evolution (Amsterdam),
June 2019, 2019-Jun, 2019-06-00, 20190601, Volume:
34, Issue:
6
Journal Article
Peer reviewed
Open access
Speciation is often thought of as a slow process due to the waiting times for mutations that cause incompatibilities, and permit ecological differentiation or assortative mating. Cases of rapid ...speciation and particularly cases of rapid adaptive radiation into multiple sympatric species have remained somewhat mysterious. We review recent findings from speciation genomics that reveal an emerging commonality among such cases: reassembly of old genetic variation into new combinations facilitating rapid speciation and adaptive radiation. The polymorphisms in old variants frequently originated from hybridization at some point in the past. We discuss why old variants are particularly good fuel for rapid speciation, and hypothesize that variation in access to such old variants might contribute to the large variation in speciation rates observed in nature.
Recent studies show that cases of rapid speciation and rapid species radiations often involve old genetic variants that arose long before the speciation events.
Old genetic variation, previously tested by selection and occurring at higher allele frequency than new mutations, is a good substrate for speciation.
Admixture variation from divergent lineages may be particularly important, potentially causing intrinsic and extrinsic incompatibilities, transgressive traits, or novel trait combinations in hybrid populations.
We review the evidence for rapid speciation involving a ‘combinatorial mechanism’ – the reassembly of old genetic variants into novel combinations.
This genetic mechanism might not only facilitate rapid speciation but also adaptive radiation and sympatric speciation, and it might contribute to variation in speciation rates among lineages.
Speciation in Freshwater Fishes Seehausen, Ole; Wagner, Catherine E
Annual review of ecology, evolution, and systematics,
11/2014, Volume:
45, Issue:
1
Journal Article
Peer reviewed
Open access
The extraordinary species richness of freshwater fishes has attracted much research on mechanisms and modes of speciation. We here review research on speciation in freshwater fishes in light of ...speciation theory, and place this in a context of broad-scale diversity patterns in freshwater fishes. We discuss several major repeated themes in freshwater fish speciation and the speciation mechanisms they are frequently associated with. These include transitions between marine and freshwater habitats, transitions between discrete freshwater habitats, and ecological transitions within habitats, as well as speciation without distinct niche shifts. Major research directions in the years to come include understanding the transition from extrinsic environment-dependent to intrinsic reproductive isolation and its influences on species persistence and understanding the extrinsic and intrinsic constraints to speciation and how these relate to broad-scale diversification patterns through time.
Adaptive radiations are bursts of evolutionary species diversification that have contributed to much of the species diversity on Earth. An exception is modern Europe, where descendants of ancient ...adaptive radiations went extinct, and extant adaptive radiations are small, recent and narrowly confined. However, not all legacy of old radiations has been lost. Subterranean environments, which are dark and food-deprived, yet buffered from climate change, have preserved ancient lineages. Here we provide evidence of an entirely subterranean adaptive radiation of the amphipod genus Niphargus, counting hundreds of species. Our modelling of lineage diversification and evolution of morphological and ecological traits using a time-calibrated multilocus phylogeny suggests a major adaptive radiation, comprised of multiple subordinate adaptive radiations. Their spatio-temporal origin coincides with the uplift of carbonate massifs in South-Eastern Europe 15 million years ago. Emerging subterranean environments likely provided unoccupied, predator-free space, constituting ecological opportunity, a key trigger of adaptive radiation. This discovery sheds new light on the biodiversity of Europe.
Does eutrophication-driven evolution change aquatic ecosystems? Alexander, Timothy J.; Vonlanthen, Pascal; Seehausen, Ole
Philosophical transactions of the Royal Society of London. Series B. Biological sciences,
01/2017, Volume:
372, Issue:
1712
Journal Article
Peer reviewed
Open access
Eutrophication increases primary production and changes the relative abundance, taxonomic composition and spatial distribution of primary producers within an aquatic ecosystem. The changes in ...composition and location of resources alter the distribution and flow of energy and biomass throughout the food web. Changes in productivity also alter the physico-chemical environment, which has further effects on the biota. Such ecological changes influence the direction and strength of natural and sexual selection experienced by populations. Besides altering selection, they can also erode the habitat gradients and/or behavioural mechanisms that maintain ecological separation and reproductive isolation among species. Consequently, eutrophication of lakes commonly results in reduced ecological specialization as well as genetic and phenotypic homogenization among lakes and among niches within lakes. We argue that the associated loss in functional diversity and niche differentiation may lead to decreased carrying capacity and lower resource-use efficiency by consumers. We show that in central European whitefish species radiations, the functional diversity affected by eutrophication-induced speciation reversal correlates with community-wide trophic transfer efficiency (fisheries yield per unit phosphorus). We take this as an example of how evolutionary dynamics driven by anthropogenic environmental change can have lasting effects on biodiversity and ecosystem functioning.
This article is part of the themed issue ‘Human influences on evolution, and the ecological and societal consequences'.
Understanding why some evolutionary lineages generate exceptionally high species diversity is an important goal in evolutionary biology. Haplochromine cichlid fishes of Africa's Lake Victoria region ...encompass >700 diverse species that all evolved in the last 150,000 years. How this 'Lake Victoria Region Superflock' could evolve on such rapid timescales is an enduring question. Here, we demonstrate that hybridization between two divergent lineages facilitated this process by providing genetic variation that subsequently became recombined and sorted into many new species. Notably, the hybridization event generated exceptional allelic variation at an opsin gene known to be involved in adaptation and speciation. More generally, differentiation between new species is accentuated around variants that were fixed differences between the parental lineages, and that now appear in many new combinations in the radiation species. We conclude that hybridization between divergent lineages, when coincident with ecological opportunity, may facilitate rapid and extensive adaptive radiation.
A fundamental challenge to our understanding of biodiversity is to explain why some groups of species undergo adaptive radiations, diversifying extensively into many and varied species, whereas ...others do not. Both extrinsic environmental factors (for example, resource availability, climate) and intrinsic lineage-specific traits (for example, behavioural or morphological traits, genetic architecture) influence diversification, but few studies have addressed how such factors interact. Radiations of cichlid fishes in the African Great Lakes provide some of the most dramatic cases of species diversification. However, most cichlid lineages in African lakes have not undergone adaptive radiations. Here we compile data on cichlid colonization and diversification in 46 African lakes, along with lake environmental features and information about the traits of colonizing cichlid lineages, to investigate why adaptive radiation does and does not occur. We find that extrinsic environmental factors related to ecological opportunity and intrinsic lineage-specific traits related to sexual selection both strongly influence whether cichlids radiate. Cichlids are more likely to radiate in deep lakes, in regions with more incident solar radiation and in lakes where there has been more time for diversification. Weak or negative associations between diversification and lake surface area indicate that cichlid speciation is not constrained by area, in contrast to diversification in many terrestrial taxa. Among the suite of intrinsic traits that we investigate, sexual dichromatism, a surrogate for the intensity of sexual selection, is consistently positively associated with diversification. Thus, for cichlids, it is the coincidence between ecological opportunity and sexual selection that best predicts whether adaptive radiation will occur. These findings suggest that adaptive radiation is predictable, but only when species traits and environmental factors are jointly considered.
Divergent natural selection has been shown to promote speciation in many taxa. However, although divergent selection often initiates the process of speciation, it often fails to complete it. Several ...time-based, geographic and genetic factors have been recognized to explain this variability in how far speciation proceeds. We review here recent evidence indicating that variability in the completeness of speciation can also be associated with the nature of divergent selection itself, with speciation being greatly promoted by (i) stronger selection on a given, single trait (the ‘stronger selection’ hypothesis) and (ii) selection on a greater number of traits (the ‘multifarious selection’ hypothesis). However, evidence for each selective hypothesis is still scarce, and further work is required to determine their relative importance.
Colonization of new ecological niches has triggered large adaptive radiations. Although some lineages have made use of such opportunities, not all do so. The factors causing this variation among ...lineages are largely unknown. Here, we show that deficiency in docosahexaenoic acid (DHA), an essential ω-3 fatty acid, can constrain freshwater colonization by marine fishes. Our genomic analyses revealed multiple independent duplications of the fatty acid desaturase gene
in stickleback lineages that subsequently colonized and radiated in freshwater habitats, but not in close relatives that failed to colonize. Transgenic manipulation of
in marine stickleback increased their ability to synthesize DHA and survive on DHA-deficient diets. Multiple freshwater ray-finned fishes also show a convergent increase in
copies, indicating its key role in freshwater colonization.
PDF
