Trends in Ecology & Evolution
ReviewA Combinatorial View on Speciation and Adaptive Radiation
Section snippets
Speciation Genomics Reveals an Important Role of Old Genetic Variants
The population genomics of speciation, ‘speciation genomics’, is a flourishing area of enquiry with much potential to address some of the big questions in speciation biology. The first generation of speciation genomics studies generated several new insights, but it is becoming clear that we are only beginning to understand the genomic basis of speciation. With the exception of a much improved understanding of the nature of genomic islands of differentiation and their link to speciation 1, 2,
The Problem: Rapid Speciation, but Slow Mutation
Many lineages accumulate species diversity at the relatively slow pace of a few new species every few million years [3]. However, some lineages appear inherently prone to rapid speciation and species radiations 4, 5, 6, 7. This leads to dramatic variation in speciation rates among lineages, and thus to highly imbalanced phylogenetic patterns of species richness [8]. Some cichlid fishes (Cichlidae) [9], some postglacial freshwater fishes (e.g., Salmonidae 10, 11), Darwin’s finches [12],
The Data: Ancient Genetic Variation Fuels Much More Recent Speciation Events
A key to understanding rapid speciation might lie in asking which loci best reflect the speciation process and in reconstructing the source of variation in these genes. Inherent to the idea of ‘speciation genes’ was a close link between the evolutionary history of alleles causing reproductive isolation [2], namely their mutational origin, and the speciation process, in other words the evolution of reproductive isolation between populations. That evolutionary history differs markedly among loci
A Combinatorial View on the Genetics of Speciation
The recent speciation genomic findings exemplified by case studies in Table 1 conflict with standard speciation models (Box 1) in many of which the origin of alleles involved in speciation marks the beginning of the speciation process. In the studies we highlight, new species evolved through new combinations of old alleles (Table 1 and Table S1 in the supplemental information online). Such a pattern is expected under an alternative set of speciation models, including recombinational speciation
Old Genetic Variation in Standing or Admixture Variation
Old genetic variation – divergent haplotypes combined into the same gene pool by hybridization or that are present as standing variation – might be a particularly good substrate for speciation compared with haplotypes that are gradually building from new mutations (Box 2). Standing genetic variation and admixture variation can represent two ends of a continuum, particularly if admixture took place in the more distant past. Similarly, in a metapopulation context, it is arbitrary whether
Admixture Variation Is a Particularly Good Substrate for Speciation
We predict that old genetic variation derived from recent hybridization (‘admixture variation’) will be more powerful than standing genetic variation in facilitating rapid speciation and species radiations. We summarize the major reasons below. All apply to speciation in general, but for rapid speciation and rapid species radiations they are likely to be particularly important.
Implications
Speciation via a combinatorial mechanism has many implications. One consequence is the decoupling of the speciation process from the slow rate of accumulation of mutations relevant to phenotypic differentiation and reproductive isolation (Figure 2 and Box 1). A second consequence is the facilitation of the evolution of linkage disequilibrium between genes even in the face of gene flow, and with it the partial alleviation of constraints to speciation imposed by sympatry [88]. Thereby, a
Concluding Remarks
Speciation through combinatorial mechanisms, by which new combinations of old gene variants quickly generate reproductively isolated species, offers a perspective on speciation that contrasts with the gradual growth of reproductive isolation through accumulation of differences generated by de novo mutations. Such a mechanism has the potential to explain how speciation can sometimes be very fast, and how multiple new species can arise nearly simultaneously and can persist in sympatry very soon
Glossary
- Adaptive radiation from a hybrid swarm
- several ecologically differentiated species evolve from a single hybrid population, wherein admixture variation not only facilitates adaptation to a variety of new niches but importantly also reproductive isolation among the emerging species.
- Balancing selection
- a selective process by which two or more alleles are maintained in the gene pool of a population at frequencies larger than expected under neutrality. Mechanisms include negative frequency-dependent
References (122)
Explosive speciation rates and unusual species richness in haplochromine cichlid fishes: effects of sexual selection
Adv. Ecol. Res.
(2000)Key innovations and the ecology of macroevolution
Trends Ecol. Evol.
(1998)- et al.
Linking color polymorphism maintenance and speciation
Trends Ecol. Evol.
(2007) Hybridization and adaptive radiation
Trends Ecol. Evol.
(2004)- et al.
Adaptation from standing genetic variation
Trends Ecol. Evol.
(2008) Multi-species outcomes in a common model of sympatric speciation
J. Theor. Biol.
(2006)The polymorphic prelude to Bateson–Dobzhansky–Muller incompatibilities
Trends Ecol. Evol.
(2012)- et al.
Understanding the onset of hybrid speciation
Trends Genet.
(2010) - et al.
Making sense of genomic islands of differentiation in light of speciation
Nat. Rev. Genet.
(2017) Interpreting the genomic landscape of speciation: a road map for finding barriers to gene flow
J. Evol. Biol.
(2017)
Speciation
The Ecology of Adaptive Radiation
Ecological opportunity and sexual selection together predict adaptive radiation
Nature
Adaptive radiation, ecological opportunity, and evolutionary determinism
Am. Nat.
Island Biology
Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation
Nat. Commun.
Rapid parallel adaptive radiations from a single hybridogenic ancestral population
Proc. R. Soc. B
Adaptive speciation in northern freshwater fishes
How and Why Species Multiply: The Radiation of Darwin’s Finches
Distinguishing noise from signal in patterns of genomic divergence in a highly polymorphic avian radiation
Mol. Ecol.
Clade-specific morphological diversification and adaptive radiation in Hawaiian songbirds
Proc. R. Soc. B
Age and rate of diversification of the Hawaiian silversword alliance (Compositae)
Proc. Natl. Acad. Sci. U. S. A.
Ecology of plant speciation
Taxon
Sexual selection and speciation: the comparative evidence revisited
Biol. Rev.
Ecological opportunity and adaptive radiation
Annu. Rev. Ecol. Evol. Syst.
Phenotypic and genetic effects of hybridization in Darwin’s finches
Evolution
Process and pattern in cichlid radiations – inferences for understanding unusually high rates of evolutionary diversification
New Phytol.
Adaptive introgression in animals: examples and comparison to new mutation and standing variation as sources of adaptive variation
Mol. Ecol.
Allopatric genetic origins for sympatric host-plant shifts and race formation in Rhagoletis
Proc. Natl. Acad. Sci.
Radiation and divergence in the Rhagoletis pomonella species complex: inferences from DNA sequence data
J. Evol. Biol.
A beak size locus in Darwin’s finches facilitated character displacement during a drought
Science
Evolution of Darwin’s finches and their beaks revealed by genome sequencing
Nature
Gene flow, ancient polymorphism, and ecological adaptation shape the genomic landscape of divergence among Darwin’s finches
Genome Res.
Speciation through sensory drive in cichlid fish
Nature
Ancient hybridization fuels rapid cichlid fish adaptive radiations
Nat. Commun.
Ancient genomic variation underlies repeated ecological adaptation in young stickleback populations
Evol. Lett.
Major ecological transitions in wild sunflowers facilitated by hybridization
Science
Ancient hybridization and phenotypic novelty within Lake Malawi’s cichlid fish radiation
Mol. Biol. Evol.
Speciation in sympatry with ongoing secondary gene flow and a potential olfactory trigger in a radiation of Cameroon cichlids
Mol. Ecol.
Disentangling incomplete lineage sorting and introgression to refine species-tree estimates for Lake Tanganyika cichlid fishes
Syst. Biol.
Phylogenomics uncovers early hybridization and adaptive loci shaping the radiation of Lake Tanganyika cichlid fishes
Nat. Commun.
Genomics of parallel ecological speciation in Lake Victoria cichlids
Mol. Biol. Evol.
Hybridisation and diversification in the adaptive radiation of clownfishes
BMC Evol. Biol.
Interspecific hybrid ancestry of a plant adaptive radiation: allopolyploidy of the Hawaiian silversword alliance (Asteraceae) inferred from floral homeotic gene duplications
Mol. Biol. Evol.
Indirect evolution of hybrid lethality due to linkage with selected locus in Mimulus guttatus
PLoS Biol.
Phylogenomics reveals three sources of adaptive variation during a rapid radiation
PLoS Biol.
Dissecting the basis of novel trait evolution in a radiation with widespread phylogenetic discordance
Mol. Ecol.
Plant Speciation
Hybrid speciation
Nature
Hybrid trait speciation and Heliconius butterflies
Philos. Trans. R. Soc. Lond. B Biol. Sci.
Cited by (0)
- †
These authors contributed equally and are listed alphabetically.