New species typically evolve over several million years. However, rates of speciation and ecological diversification vary by orders of magnitude across the tree of life, with the fastest shown by some adaptive radiations. Eight hundred endemic species of cichlid fishes emerged and formed entire food webs in Lake Victoria and nearby lakes in East Africa. According to Victorias paleolimnological history, five hundred may have arisen within the past 16,700 years, but molecular phylogenies estimated a much older origin. We reconstruct the age and demography of all Lake Victoria region radiations from whole genomes. We show that indeed, in Lake Victoria all trophic guilds diverged <16,700 years ago, corresponding to between 537 and nearly 30000 speciation events per species per million years, the fastest speciation rate in metazoans. Cichlid radiations in lakes Edward, Albert and Kivu too began <20,000 years ago, an order of magnitude faster than previously thought. Evolutionary transitions between trophic levels led to divergence in effective population sizes as predicted by the trophic pyramid of numbers concept and replicated across three parallel food web radiations. Our results demonstrate that classical theory of trophic interactions in ecologically assembled food webs applies equally to food webs that assembled through rapid adaptive radiation. ### Competing Interest Statement The authors have declared no competing interest.

Adaptive radiations highlight the mechanisms by which species and traits diversify and the extent to which these patterns are predictable. We used 1,110 high-speed videos of suction feeding to study functional and morphological diversification in 300 cichlid species from three African Great Lake radiations of varying ages (Victoria, Malawi, and Tanganyika) and an older, spatially dispersed continental radiation in the Neotropics. Among African radiations, standing diversity was reflective of time. Morphological and functional variance in Lake Victoria, the youngest radiation, was a subset of that within Lake Malawi, which itself was nested within the older Tanganyikan radiation. However, functional diversity in Neotropical cichlids was often lower than that in Lake Tanganyika, despite being much older. These two radiations broadly overlapped, but each diversified into novel trait spaces not found in the youngest lake radiations. Evolutionary rates across radiations were inversely related to age, suggesting extremely rapid trait evolution at early stages, particularly in lake radiations. Despite this support for early bursts, other patterns of trait diversity were inconsistent with expectations of adaptive radiations. This work suggests that cichlid functional evolution has played out in strikingly similar fashion in different radiations, with contingencies eventually resulting in lineage-specific novelties.

Key innovations, traits that provide species access to novel niches, are thought to be a major generator of biodiversity. One commonly cited example of key innovation is pharyngognathy, a set of modifications to the pharyngeal jaws found in some highly species-rich fish clades such as cichlids and wrasses. Here, using comparative phylogenomics and phylogenetic comparative methods, we investigate the genomic basis of pharyngognathy and the impact of this innovation on diversification. Whole genomes resolve the relationships of fish clades with this innovation and their close relatives, but high levels of topological discordance suggest the innovation may have evolved fewer times than previously thought. Closer examination of the topology of noncoding elements accelerated in clades with the pharyngognathy innovation reveals hidden patterns of shared ancestry across putatively independent transitions to pharyngognathy. When our updated phylogenomic relationships are used alongside large-scale phylogenetic and ecological datasets, we find no evidence pharyngognathy consistently modifies the macroevolutionary landscape of trophic ecology nor does it increase diversification. Our results highlight the necessity of incorporating genomic information in studies of key innovation. Key innovations are traits that trigger the rapid evolution of new species occupying novel niches. Fresh genetic evidence reveals that the modified throat jaws of some fishes, thought to be a textbook example of key innovation, have a complex history that does not fit the classic definition.

Birdsongs are among the most distinctive animal signals. Their evolution is thought to be shaped simultaneously by habitat structure and by the constraints of morphology. Habitat structure affects song transmission and detectability, thus influencing song (the acoustic adaptation hypothesis), while body size and beak size and shape necessarily constrain song characteristics (the morphological constraint hypothesis). Yet, support for the acoustic adaptation and morphological constraint hypotheses remains equivocal, and their simultaneous examination is infrequent. Using a phenotypically diverse Australasian bird clade, the honeyeaters (Aves: Meliphagidae), we compile a dataset consisting of song, environmental, and morphological variables for 163 species and jointly examine predictions of these two hypotheses. Overall, we find that body size constrains song frequency and pace in honeyeaters. Although habitat type and environmental temperature influence aspects of song, that influence is indirect, likely via effects of environmental variation on body size, with some evidence that elevation constrains the evolution of song peak frequency. Our results demonstrate that morphology has an overwhelming influence on birdsong, in support of the morphological constraint hypothesis, with the environment playing a secondary role generally via body size rather than habitat structure. These results suggest that changing body size (a consequence of both global effects such as climate change and local effects such as habitat transformation) will substantially influence the nature of birdsong.

Crater lake fishes are common evolutionary model systems, with recent studies suggesting a key role for gene flow in promoting rapid adaptation and speciation. However, the study of these young lakes can be complicated by human-mediated extinctions. Museum genomics approaches integrating genetic data from recently extinct species are, therefore, critical to understanding the complex evolutionary histories of these fragile systems. Here, we examine the evolutionary history of an extinct Southern Hemisphere crater lake endemic, the rainbowfish Melanotaenia eachamensis. We undertook a comprehensive sampling of extant rainbowfish populations of the Atherton Tablelands of Australia alongside historical museum material to understand the evolutionary origins of the extinct crater lake population and the dynamics of gene flow across the ecoregion. The extinct crater lake species is genetically distinct from all other nearby populations due to historic introgression between 2 proximate riverine lineages, similar to other prominent crater lake speciation systems, but this historic gene flow has not been sufficient to induce a species flock. Our results suggest that museum genomics approaches can be successfully combined with extant sampling to unravel complex speciation dynamics involving recently extinct species.

Background Viviparity—live birth—is a complex and innovative mode of reproduction that has evolved repeatedly across the vertebrate Tree of Life. Viviparous species exhibit remarkable levels of reproductive diversity, both in the amount of care provided by the parent during gestation, and the ways in which that care is delivered. The genetic basis of viviparity has garnered increasing interest over recent years; however, such studies are often undertaken on small evolutionary timelines, and thus are not able to address changes occurring on a broader scale. Using whole genome data, we investigated the molecular basis of this innovation across the diversity of vertebrates to answer a long held question in evolutionary biology: is the evolution of convergent traits driven by convergent genomic changes? Results We reveal convergent changes in protein family sizes, protein-coding regions, introns, and untranslated regions (UTRs) in a number of distantly related viviparous lineages. Specifically, we identify 15 protein families showing evidence of contraction or expansion associated with viviparity. We additionally identify elevated substitution rates in both coding and noncoding sequences in several viviparous lineages. However, we did not find any convergent changes—be it at the nucleotide or protein level—common to all viviparous lineages. Conclusions Our results highlight the value of macroevolutionary comparative genomics in determining the genomic basis of complex evolutionary transitions. While we identify a number of convergent genomic changes that may be associated with the evolution of viviparity in vertebrates, there does not appear to be a convergent molecular signature shared by all viviparous vertebrates. Ultimately, our findings indicate that a complex trait such as viviparity likely evolves with changes occurring in multiple different pathways.

The evolutionary history of Southern Hemisphere graylings (Retropinnidae) in Aotearoa New Zealand—including the number of colonisation events, the directionality and timing of dispersal, and their relationship to the Australian grayling—is poorly understood. The New Zealand grayling ( Prototroctes oxyrhynchus ) is the only known freshwater fish species to have gone extinct since human arrival in New Zealand. Despite its historical abundance, only 23 formalin-fixed specimens (both wet and dried) exist in museum collections globally, which were previously non-amenable to palaeogenetic analysis. Here, we used high-throughput DNA sequencing techniques, specifically designed for formalin-fixed specimens, to generate mitochondrial genomes of P. oxyrhynchus , and analysed these within a temporal phylogenetic framework of retropinnid and osmerid taxa. We recovered strong evidence for a sister relationship between the New Zealand and Australian grayling ( P. mareana ), with the two having a common ancestor around 13.8 Mya (95% HPD: 6.1–23.2 Mya), after the height of Oligocene marine inundation in New Zealand. Our temporal phylogenetic analysis suggests a single marine dispersal event between New Zealand and Australia, though the direction of dispersal is equivocal, followed by divergence into genetically and morphologically distinguishable species through isolation by distance. This study provides further insights into the possible drivers of the extinction of the New Zealand grayling, and highlights how advancements in palaeogenetic techniques can be used to test evolutionary hypotheses in extinct (and living) fish, which have been comparatively neglected in the field of ancient DNA.

Although some lineages of animals and plants have made impressive adaptive radiations when provided with ecological opportunity, the propensities to radiate vary profoundly among lineages for unknown reasons. In Africa's Lake Victoria region, one cichlid lineage radiated in every lake, with the largest radiation taking place in a lake less than 16,000 years old. We show that all of its ecological guilds evolved in situ. Cycles of lineage fusion through admixture and lineage fission through speciation characterize the history of the radiation. It was jump-started when several swamp-dwelling refugial populations, each of which were of older hybrid descent, met in the newly forming lake, where they fused into a single population, resuspending old admixture variation. Each population contributed a different set of ancient alleles from which a new adaptive radiation assembled in record time, involving additional fusion-fission cycles. We argue that repeated fusion-fission cycles in the history of a lineage make adaptive radiation fast and predictable.

Birdsongs are well-known acoustic signals and are thought to play a key role in sexual selection. Despite the established role of birdsong in sexual selection and reproductive isolation at microevolutionary scales, its macroevolutionary impacts on clade diversification remain largely unexplored. Here, we test the hypothesis that shifts in song evolution influence diversification using honeyeaters, a diverse clade of songbirds restricted to Australasia. Using song data for 163 honeyeater species, we employ phylogenetic comparative models of trait evolution to detect shifts in optima for song evolution and use hidden state-dependent speciation and extinction models to assess the influence of these shifts on diversification. Contrary to our expectations, we find no correlation between shifts in song evolution and shifts in diversification rates, and models suggest other factors play a role. Overall, shifts in song evolution do not significantly contribute to diversification in honeyeaters, likely due to other ecological factors influencing diversification in this group including range size and dispersal ability.### Competing Interest StatementThe authors have declared no competing interest.

Background Darwin and others proposed that a species’ geographic range size positively influences speciation likelihood, with the relationship potentially dependent on the mode of speciation and other contributing factors, including geographic setting and species traits. Several alternative proposals for the influence of range size on speciation rate have also been made (e.g. negative or a unimodal relationship with speciation). To examine Darwin’s proposal, we use a range of phylogenetic comparative methods, focusing on a large Australasian bird clade, the honeyeaters (Aves: Meliphagidae). Results We consider the influence of range size, shape, and position (latitudinal and longitudinal midpoints, island or continental species), and consider two traits known to influence range size: dispersal ability and body size. Applying several analytical approaches, including phylogenetic Bayesian path analysis, spatiophylogenetic models, and state-dependent speciation and extinction models, we find support for both the positive relationship between range size and speciation rate and the influence of mode of speciation. Conclusions Honeyeater speciation rate differs considerably between islands and the continental setting across the clade’s distribution, with range size contributing positively in the continental setting, while dispersal ability influences speciation regardless of setting. These outcomes support Darwin’s original proposal for a positive relationship between range size and speciation likelihood, while extending the evidence for the contribution of dispersal ability to speciation.

Hybrid incompatibilities occur when interactions between opposite ancestry alleles at different loci reduce the fitness of hybrids. Most work on incompatibilities has focused on those that are "intrinsic," meaning they affect viability and sterility in the laboratory. Theory predicts that ecological selection can also underlie hybrid incompatibilities, but tests of this hypothesis using sequence data are scarce. In this article, we compiled genetic data for F-2 hybrid crosses between divergent populations of threespine stickleback fish (Gasterosteus aculeatus L.) that were born and raised in either the field (seminatural experimental ponds) or the laboratory (aquaria). Because selection against incompatibilities results in elevated ancestry heterozygosity, we tested the prediction that ancestry heterozygosity will be higher in pond-raised fish compared to those raised in aquaria. We found that ancestry heterozygosity was elevated by approximately 3% in crosses raised in ponds compared to those raised in aquaria. Additional analyses support a phenotypic basis for incompatibility and suggest that environment-specific single-locus heterozygote advantage is not the cause of selection on ancestry heterozygosity. Our study provides evidence that, in stickleback, a coarse-albeit indirect-signal of environment-dependent hybrid incompatibility is reliably detectable and suggests that extrinsic incompatibilities can evolve before intrinsic incompatibilities.

Identification of particular traits that predispose species to elevated extinction risk is an important component of proactive conservation. We capitalise on a recent strategic extinction risk assessment of all Australian squamate reptiles to identify intrinsic life history traits and extrinsic threats that correlate with extinction risk. We further assess whether extinction risk correlates differ between species impacted by different threatening processes (habitat loss vs. invasive species).

Hybrid incompatibilities occur when interactions between opposite-ancestry alleles at different loci reduce the fitness of hybrids. Most work on incompatibilities has focused on those that are ‘intrinsic’, meaning they affect viability and sterility in the laboratory. Theory predicts that ecological selection can also underlie hybrid incompatibilities, but tests of this hypothesis are scarce. In this article, we compiled genetic data for F2hybrid crosses between divergent populations of threespine stickleback fish (Gasterosteus aculeatusL.) that were born and raised in either the field (semi-natural experimental ponds) or the laboratory (aquaria). We tested for differences in excess heterozygosity between these two environments at ancestry informative loci—a genetic signature of selection against incompatibilities. We found that excess ancestry heterozygosity was elevated by approximately 3% in crosses raised in ponds compared to those raised in aquaria. Previous results from F1 hybrids in the field suggest that pond-specific (single-locus) heterosis is unlikely to explain this finding. Our study suggests that, in stickleback, a coarse signal of environment-dependent hybrid incompatibilities is reliably detectable and that extrinsic incompatibilities have evolved before intrinsic incompatibilities.

Adaptive radiations are generally thought to occur soon after a lineage invades a region offering high levels of ecological opportunity. However, few adaptive radiations beyond a handful of exceptional examples are known, so a comprehensive understanding of their dynamics is still lacking. Here, we present a novel case of an island species flock of freshwater fishes with a radically different tempo of adaptive history than that found in many popular evolutionary model systems. Using a phylogenomic data set combined with simultaneous Bayesian estimation of divergence times and trait-based speciation and extinction models, we show that the New Zealand Gobiomorphus gudgeons comprise a monophyletic assemblage, but surprisingly, the radiation did not fully occupy freshwater habitats and explosively speciate until more than 10 myr after the lineage invaded the islands. This shift in speciation rate was not accompanied by an acceleration in the rate of morphological evolution in the freshwater crown clade relative to the other species, but is correlated with a reduction in head pores and scales as well as an increase in egg size. Our results challenge the notion that clades always rapidly exploit ecological opportunities in the absence of competing lineages. Instead, we demonstrate that adaptive radiation can experience a slow start before undergoing accelerated diversification and that lineage and phenotypic diversification may be uncoupled in young radiations. [Adaptive radiation; Eleotridae; freshwater; Gobiomorphus; New Zealand.].

This month’s Genome Watch highlights how the search for the origins of SARS-CoV-2 emphasizes the need for integrated phylogenetic methods. This month’s Genome Watch highlights how the search for the origins of SARS-CoV-2 emphasizes the need for integrated phylogenetic methods.

Abstract The East African cichlid radiations are characterized by repeated and rapid diversification into many distinct species with different ecological specializations and by a history of hybridization events between nonsister species. Such hybridization might provide important fuel for adaptive radiation. Interspecific hybrids can have extreme trait values or novel trait combinations and such transgressive phenotypes may allow some hybrids to explore ecological niches neither of the parental species could tap into. Here, we investigate the potential of second‐generation (F2) hybrids between two generalist cichlid species from Lake Malawi to exploit a resource neither parental species is specialized on: feeding by sifting sand. Some of the F2 hybrids phenotypically resembled fish of species that are specialized on sand sifting. We combined experimental behavioral and morphometric approaches to test whether the F2 hybrids are transgressive in both morphology and behavior related to sand sifting. We then performed a quantitative trait loci (QTL) analysis using RADseq markers to investigate the genetic architecture of morphological and behavioral traits. We show that transgression is present in several morphological traits, that novel trait combinations occur, and we observe transgressive trait values in sand sifting behavior in some of the F2 hybrids. Moreover, we find QTLs for morphology and for sand sifting behavior, suggesting the existence of some loci with moderate to large effects. We demonstrate that hybridization has the potential to rapidly generate novel and ecologically relevant phenotypes that may be suited to a niche neither of the parental species occupies. Interspecific hybridization may thereby contribute to the rapid generation of ecological diversity in cichlid radiations.

Speciation rates vary considerably among lineages, and our understanding of what drives the rapid succession of speciation events within young adaptive radiations remains incomplete1–11. The cichlid fish family provides a notable example of such variation, with many slowly speciating lineages as well as several exceptionally large and rapid radiations12. Here, by reconstructing a large phylogeny of all currently described cichlid species, we show that explosive speciation is solely concentrated in species flocks of several large young lakes. Increases in the speciation rate are associated with the absence of top predators; however, this does not sufficiently explain explosive speciation. Across lake radiations, we observe a positive relationship between the speciation rate and enrichment of large insertion or deletion polymorphisms. Assembly of 100 cichlid genomes within the most rapidly speciating cichlid radiation, which is found in Lake Victoria, reveals exceptional ‘genomic potential’—hundreds of ancient haplotypes bear insertion or deletion polymorphisms, many of which are associated with specific ecologies and shared with ecologically similar species from other older radiations elsewhere in Africa. Network analysis reveals fundamentally non-treelike evolution through recombining old haplotypes, and the origins of ecological guilds are concentrated early in the radiation. Our results suggest that the combination of ecological opportunity, sexual selection and exceptional genomic potential is the key to understanding explosive adaptive radiation. Analyses of the genomes of cichlid species reveal that the combination of ecological opportunity, sexual selection and exceptional genomic potential is the key to understanding explosive adaptive radiation in cichlids.

EthologyVolume 125, Issue 11 p. 851-854 COMMENTARY Insufficient data render comparative analyses of the evolution of cooperative breeding mere speculation: A reply to Dey et al. Michael Taborsky, Michael Taborsky orcid.org/0000-0002-1357-4316 Institute of Ecology and Evolution, University of Bern, Hinterkappelen, SwitzerlandSearch for more papers by this authorStephan Koblmüller, Stephan Koblmüller orcid.org/0000-0002-1024-3220 Institute of Biology, University of Graz, Graz, AustriaSearch for more papers by this authorKristina M. Sefc, Kristina M. Sefc orcid.org/0000-0001-8108-8339 Institute of Biology, University of Graz, Graz, AustriaSearch for more papers by this authorMatthew McGee, Matthew McGee Monash University, Melbourne, Victoria, AustraliaSearch for more papers by this authorMasanori Kohda, Masanori Kohda Department of Biology and Geosciences, Osaka City University, Osaka, JapanSearch for more papers by this authorSatoshi Awata, Satoshi Awata Department of Biology and Geosciences, Osaka City University, Osaka, JapanSearch for more papers by this authorMichio Hori, Michio Hori Department of Zoology, Kyoto University, Kyoto, JapanSearch for more papers by this authorJoachim G. Frommen, Corresponding Author Joachim G. Frommen joachim.frommen@iee.unibe.ch orcid.org/0000-0002-1752-6944 Institute of Ecology and Evolution, University of Bern, Hinterkappelen, Switzerland Correspondence Joachim G. Frommen, Institute of Ecology and Evolution, University of Bern, Wohlenstrasse 50A, 3032 Hinterkappelen, Switzerland. Email: joachim.frommen@iee.unibe.chSearch for more papers by this author Michael Taborsky, Michael Taborsky orcid.org/0000-0002-1357-4316 Institute of Ecology and Evolution, University of Bern, Hinterkappelen, SwitzerlandSearch for more papers by this authorStephan Koblmüller, Stephan Koblmüller orcid.org/0000-0002-1024-3220 Institute of Biology, University of Graz, Graz, AustriaSearch for more papers by this authorKristina M. Sefc, Kristina M. Sefc orcid.org/0000-0001-8108-8339 Institute of Biology, University of Graz, Graz, AustriaSearch for more papers by this authorMatthew McGee, Matthew McGee Monash University, Melbourne, Victoria, AustraliaSearch for more papers by this authorMasanori Kohda, Masanori Kohda Department of Biology and Geosciences, Osaka City University, Osaka, JapanSearch for more papers by this authorSatoshi Awata, Satoshi Awata Department of Biology and Geosciences, Osaka City University, Osaka, JapanSearch for more papers by this authorMichio Hori, Michio Hori Department of Zoology, Kyoto University, Kyoto, JapanSearch for more papers by this authorJoachim G. Frommen, Corresponding Author Joachim G. Frommen joachim.frommen@iee.unibe.ch orcid.org/0000-0002-1752-6944 Institute of Ecology and Evolution, University of Bern, Hinterkappelen, Switzerland Correspondence Joachim G. Frommen, Institute of Ecology and Evolution, University of Bern, Wohlenstrasse 50A, 3032 Hinterkappelen, Switzerland. Email: joachim.frommen@iee.unibe.chSearch for more papers by this author First published: 25 July 2019 https://doi.org/10.1111/eth.12929Citations: 8Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat Citing Literature Volume125, Issue11November 2019Pages 851-854 RelatedInformation

Identifying traits that underlie variation in individual performance of consumers (i.e., trait utility) can help reveal the ecological causes of population divergence and the subsequent consequences for species interactions and community structure. Here, we document a case of rapid divergence (over the past 100 generations, or ∼150 years) in foraging traits and feeding efficiency between a lake and stream population pair of threespine stickleback. Building on predictions from functional trait models of fish feeding, we analyzed foraging experiments with a Bayesian path analysis and elucidated the traits explaining variation in foraging performance and the species composition of ingested prey. Despite extensive previous research on the divergence of foraging traits among populations and ecotypes of stickleback, our results provide novel experimental evidence of trait utility for jaw protrusion, gill raker length, and gill raker spacing when foraging on a natural zooplankton assemblage. Furthermore, we discuss how these traits might contribute to the differential effects of lake and stream stickleback on their prey communities, observed in both laboratory and mesocosm conditions. More generally, our results illustrate how the rapid divergence of functional foraging traits of consumers can impact the biomass, species composition, and trophic structure of prey communities.

Trophic ecology is thought to exert a profound influence on biodiversity, but the specifics of the process are rarely examined at large spatial and evolutionary scales. We investigate how trophic position and diet breadth influence functional trait evolution in one of the most species-rich and complex vertebrate assemblages, coral reef fishes, within a large-scale phylogenetic framework. We show that, in contrast with established theory, functional traits evolve fastest in trophic specialists with narrow diet breadths at both very low and high trophic positions. Top trophic level specialists exhibit the most functional diversity, while omnivorous taxa with intermediate trophic positions and wide diet breadth have the least functional diversity. Our results reveal the importance of trophic position in shaping evolutionary dynamics while simultaneously highlighting the incredible trophic and functional diversity present in coral reef fish assemblages.