A continuous fish fossil record reveals key insights into adaptive radiation.

Adaptive radiations have been instrumental in generating a considerable amount of life's diversity. Ecological opportunity is thought to be a prerequisite for adaptive radiation1, but little is known about the relative importance of species' ecological versatility versus effects of arrival order in determining which lineage radiates2. Palaeontological records that could help answer this are scarce. In Lake Victoria, a large adaptive radiation of cichlid fishes evolved in an exceptionally short and recent time interval3. We present a rich continuous fossil record extracted from a series of long sediment cores along an onshore-offshore gradient. We reconstruct the temporal sequence of events in the assembly of the fish community from thousands of tooth fossils. We reveal arrival order, relative abundance and habitat occupation of all major fish lineages in the system. We show that all major taxa arrived simultaneously as soon as the modern lake began to form. There is no evidence of the radiating haplochromine cichlid lineage arriving before others, nor of their numerical dominance upon colonization; therefore, there is no support for ecological priority effects. However, although many taxa colonized the lake early and several became abundant, only cichlids persisted in the new deep and open-water habitats once these emerged. Because these habitat gradients are also known to have played a major role in speciation, our findings are consistent with the hypothesis that ecological versatility was key to adaptive radiation, not priority by arrival order nor initial numerical dominance.

The ecological and genomic basis of explosive adaptive radiation.

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.

Sympatry and parapatry among rocky reef cichlids of Lake Victoria explained by female mating preferences.

Work on the Lake Victoria cichlids Pundamilia nyererei (red dorsum males, deeper water), Pundamilia pundamilia (blue males, shallower water) and related species pairs has provided insights into processes of speciation. Here, we investigate the female mating behaviour of 5 Pundamilia species and 4 of their F1 hybrids through mate choice trials and paternity testing. Complete assortative mating was observed among all sympatric species. Parapatric species with similar depth habitat distributions interbred whereas other parapatric and allopatric species showed complete assortative mating. F1 hybrids mated exclusively with species accepted by females of the parental species. The existence of complete assortative mating among some currently allopatric species suggests that pre-existing mating barriers could be sufficient to explain current patterns of co-existence, although, of course, many other factors may be involved. Regardless of the mechanism, mating preferences may influence species distribution in potentially hybridizing taxa, such as in the adaptive radiation of cichlid fish. We suggest that this at least partly explains why some species fail to establish breeding populations in locations where they are occasionally recorded. Our results support the notion that the mating preferences of potentially cross-breeding species ought to be included in coexistence theory.

Testing alternative hypotheses for the decline of cichlid fish in Lake Victoria using fish tooth time series from sediment cores.

Lake Victoria is well known for its high diversity of endemic fish species and provides livelihoods for millions of people. The lake garnered widespread attention during the twentieth century as major environmental and ecological changes modified the fish community with the extinction of approximately 40% of endemic cichlid species by the 1980s. Suggested causal factors include anthropogenic eutrophication, fishing, and introduced non-native species but their relative importance remains unresolved, partly because monitoring data started in the 1970s when changes were already underway. Here, for the first time, we reconstruct two time series, covering the last approximately 200 years, of fish assemblage using fish teeth preserved in lake sediments. Two sediment cores from the Mwanza Gulf of Lake Victoria, were subsampled continuously at an intra-decadal resolution, and teeth were identified to major taxa: Cyprinoidea, Haplochromini, Mochokidae and Oreochromini. None of the fossils could be confidently assigned to non-native Nile perch. Our data show significant decreases in haplochromine and oreochromine cichlid fish abundances that began long before the arrival of Nile perch. Cyprinoids, on the other hand, have generally been increasing. Our study is the first to reconstruct a time series of any fish assemblage in Lake Victoria extending deeper back in time than the past 50 years, helping shed light on the processes underlying Lake Victoria's biodiversity loss.

Linking human impacts to community processes in terrestrial and freshwater ecosystems.

Human impacts such as habitat loss, climate change and biological invasions are radically altering biodiversity, with greater effects projected into the future. Evidence suggests human impacts may differ substantially between terrestrial and freshwater ecosystems, but the reasons for these differences are poorly understood. We propose an integrative approach to explain these differences by linking impacts to four fundamental processes that structure communities: dispersal, speciation, species-level selection and ecological drift. Our goal is to provide process-based insights into why human impacts, and responses to impacts, may differ across ecosystem types using a mechanistic, eco-evolutionary comparative framework. To enable these insights, we review and synthesise (i) how the four processes influence diversity and dynamics in terrestrial versus freshwater communities, specifically whether the relative importance of each process differs among ecosystems, and (ii) the pathways by which human impacts can produce divergent responses across ecosystems, due to differences in the strength of processes among ecosystems we identify. Finally, we highlight research gaps and next steps, and discuss how this approach can provide new insights for conservation. By focusing on the processes that shape diversity in communities, we aim to mechanistically link human impacts to ongoing and future changes in ecosystems.

Introgression from extinct species facilitates adaptation to its vacated niche.

Anthropogenic disturbances of ecosystems are causing a loss of biodiversity at an unprecedented rate. Species extinctions often leave ecological niches underutilized, and their colonization by other species may require new adaptation. In Lake Constance, on the borders of Germany, Austria and Switzerland, an endemic profundal whitefish species went extinct during a period of anthropogenic eutrophication. In the process of extinction, the deep-water species hybridized with three surviving whitefish species of Lake Constance, resulting in introgression of genetic variation that is potentially adaptive in deep-water habitats. Here, we sampled a water depth gradient across a known spawning ground of one of these surviving species, Coregonus macrophthalmus, and caught spawning individuals at greater depths (down to 90 m) than historically recorded. We sequenced a total of 96 whole genomes, 11-17 for each of six different spawning depth populations (4, 12, 20, 40, 60 and 90 m), to document genomic intraspecific differentiation along a water depth gradient. We identified 52 genomic regions that are potentially under divergent selection between the deepest (90 m) and all shallower (4-60 m) spawning habitats. At 12 (23.1%) of these 52 loci, the allele frequency pattern across historical and contemporary populations suggests that introgression from the extinct species potentially facilitates ongoing adaptation to deep water. Our results are consistent with the syngameon hypothesis, proposing that hybridization between members of an adaptive radiation can promote further niche expansion and diversification. Furthermore, our findings demonstrate that introgression from extinct into extant species can be a source of evolvability, enabling rapid adaptation to environmental change, and may contribute to the ecological recovery of ecosystem functions after extinctions.

Long-wavelength-sensitive (lws) opsin gene expression, foraging and visual communication in coral reef fishes.

Coral reef fishes are diverse in ecology and behaviour and show remarkable colour variability. Investigating the visual pigment gene (opsin) expression in these fishes makes it possible to associate their visual genotype and phenotype (spectral sensitivities) to visual tasks, such as feeding strategy or conspecific detection. By studying all major damselfish clades (Pomacentridae) and representatives from five other coral reef fish families, we show that the long-wavelength-sensitive (lws) opsin is highly expressed in algivorous and less or not expressed in zooplanktivorous species. Lws is also upregulated in species with orange/red colours (reflectance >520 nm) and expression is highest in orange/red-coloured algivores. Visual models from the perspective of a typical damselfish indicate that sensitivity to longer wavelengths does enhance the ability to detect the red to far-red component of algae and orange/red-coloured conspecifics, possibly enabling social signalling. Character state reconstructions indicate that in the early evolutionary history of damselfishes, there was no lws expression and no orange/red coloration. Omnivory was most often the dominant state. Although herbivory was sometimes dominant, zooplanktivory was never dominant. Sensitivity to long wavelength (increased lws expression) only emerged in association with algivory but never with zooplanktivory. Higher lws expression is also exploited by social signalling in orange/red, which emerged after the transition to algivory. Although the relative timing of traits may deviate by different reconstructions and alternative explanations are possible, our results are consistent with sensory bias whereby social signals evolve as a correlated response to natural selection on sensory system properties in other contexts.

Ancient DNA is preserved in fish fossils from tropical lake sediments.

Tropical freshwater lakes are well known for their high biodiversity, and particularly the East African Great Lakes are renowned for their adaptive radiation of cichlid fishes. While comparative phylogenetic analyses of extant species flocks have revealed patterns and processes of their diversification, little is known about evolutionary trajectories within lineages, the impacts of environmental drivers, or the scope and nature of now-extinct diversity. Time-structured palaeodata from geologically young fossil records, such as fossil counts and particularly ancient DNA (aDNA) data, would help fill this large knowledge gap. High ambient temperatures can be detrimental to the preservation of DNA, but refined methodology now allows data generation even from very poorly preserved samples. Here, we show for the first time that fish fossils from tropical lake sediments yield endogenous aDNA. Despite generally low endogenous content and high sample dropout, the application of high-throughput sequencing and, in some cases, sequence capture allowed taxonomic assignment and phylogenetic placement of 17% of analysed fish fossils to family or tribe level, including remains which are up to 2700 years old or weigh less than 1 mg. The relationship between aDNA degradation and the thermal age of samples is similar to that described for terrestrial samples from cold environments when adjusted for elevated temperature. Success rates and aDNA preservation differed between the investigated lakes Chala, Kivu and Victoria, possibly caused by differences in bottom water oxygenation. Our study demonstrates that the sediment records of tropical lakes can preserve genetic information on rapidly diversifying fish taxa over time scales of millennia.

Environmentally independent selection for hybrids between divergent freshwater stickleback lineages in semi-natural ponds.

Hybridization following secondary contact of genetically divergent populations can influence the range expansion of invasive species, though specific outcomes depend on the environmental dependence of hybrid fitness. Here, using two genetically and ecologically divergent threespine stickleback lineages that differ in their history of freshwater colonization, we estimate fitness variation of parental lineages and hybrids in semi-natural freshwater ponds with contrasting histories of nutrient loading. In our experiment, we found that fish from the older freshwater lineage (Lake Geneva) and hybrids outperformed fish from the younger freshwater lineage (Lake Constance) in terms of both growth and survival, regardless of the environmental context of our ponds. Across all ponds, hybrids exhibited the highest survival. Although wild-caught adult populations differed in their functional and defence morphology, it is unclear which of these traits underlie the fitness differences observed among juveniles in our experiment. Overall, our work suggests that when hybrid fitness is insensitive to environmental conditions, as observed here, introgression may promote population expansion into unoccupied habitats and accelerate invasion success.

The enrichment paradox in adaptive radiations: Emergence of predators hinders diversification in resource rich environments.

Adaptive radiations are known for rapid niche diversification in response to ecological opportunity. While most resources usually exist prior to adaptive radiation, novel niches associated with novel resources can be created as a clade diversifies. For example, in African lake cichlid radiations some species prey upon other species of the clade (intraclade consumers). Using a trait-based eco-evolutionary model, we investigate the evolution of intraclade consumers in adaptive radiations and the effect of this novel trophic interaction on the diversification process of the radiating clade. We find that the evolutionary emergence of intraclade consumers halts the diversification processes of other ecomorphs as a result of increased top-down control of density. Because high productivity enables earlier evolution of intraclade consumers, highly productive environments come to harbour less species-rich radiations than comparable radiations in less productive environments. Our results reveal how macroevolutionary and community patterns can emerge from ecological and microevolutionary processes.

Competition among small individuals hinders adaptive radiation despite ecological opportunity.

Ontogenetic diet shifts, where individuals change their resource use during development, are the rule rather than the exception in the animal world. Here, we aim to understand how such changes in diet during development affect the conditions for an adaptive radiation in the presence of ecological opportunity. We use a size-structured consumer-resource model and the adaptive dynamics approach to study the ecological conditions for speciation. We assume that small individuals all feed on a shared resource. Large individuals, on the other hand, have access to multiple food sources on which they can specialize. We find that competition among small individuals can hinder an adaptive radiation to unfold, despite plenty of ecological opportunity for large individuals. When small individuals experience strong competition for food, they grow slowly and only a few individuals are recruited to the larger size classes. Hence, competition for food among large individuals is weak and there is therefore no disruptive selection. In addition, initial conditions determine if an adaptive radiation occurs or not. A consumer population initially dominated by small individuals will not radiate. On the other hand, a population initially dominated by large individuals may undergo adaptive radiation and diversify into multiple species.

Genetic architecture of adaptive radiation across two trophic levels.

Evolution of trophic diversity is a hallmark of adaptive radiation. Yet, transitions between carnivory and herbivory are rare in young adaptive radiations. Haplochromine cichlid fish of the African Great Lakes are exceptional in this regard. Lake Victoria was colonized by an insectivorous generalist and in less than 20 000 years, several clades of specialized herbivores evolved. Carnivorous versus herbivorous lifestyles in cichlids require many different adaptations in functional morphology, physiology and behaviour. Ecological transitions in either direction thus require many traits to change in a concerted fashion, which could be facilitated if genomic regions underlying these traits were physically linked or pleiotropic. However, linkage/pleiotropy could also constrain evolvability. To investigate components of the genetic architecture of a suite of traits that distinguish invertivores from algae scrapers, we performed quantitative trait locus (QTL) mapping using a second-generation hybrid cross. While we found indications of linkage/pleiotropy within trait complexes, QTLs for distinct traits were distributed across several unlinked genomic regions. Thus, a mixture of independently segregating variation and some pleiotropy may underpin the rapid trophic transitions. We argue that the emergence and maintenance of associations between the different genomic regions underpinning co-adapted traits that evolved and persist against some gene flow required reproductive isolation.

Climate, immigration and speciation shape terrestrial and aquatic biodiversity in the European Alps.

Quaternary climate fluctuations can affect speciation in regional biodiversity assembly in two non-mutually exclusive ways: a glacial species pump, where isolation in glacial refugia accelerates allopatric speciation, and adaptive radiation in underused adaptive zones during ice-free periods. We detected biogeographic and genetic signatures associated with both mechanisms in the assembly of the biota of the European Alps. Age distributions of endemic and widespread species within aquatic and terrestrial taxa (amphipods, fishes, amphibians, butterflies and flowering plants) revealed that endemic fish evolved only in lakes, are highly sympatric, and mainly of Holocene age, consistent with adaptive radiation. Endemic amphipods are ancient, suggesting preglacial radiation with limited range expansion and local Pleistocene survival, perhaps facilitated by a groundwater-dwelling lifestyle. Terrestrial endemics are mostly of Pleistocene age and are thus more consistent with the glacial species pump. The lack of evidence for Holocene adaptive radiation in the terrestrial biome is consistent with faster recolonization through range expansion of these taxa after glacial retreats. More stable and less seasonal ecological conditions in lakes during the Holocene may also have contributed to Holocene speciation in lakes. The high proportion of young, endemic species makes the Alpine biota vulnerable to climate change, but the mechanisms and consequences of species loss will likely differ between biomes because of their distinct evolutionary histories.

Multispecies colour polymorphisms associated with contrasting microhabitats in two Mediterranean wrasse radiations.

Intraspecific colour polymorphisms (CPs) present unique opportunities to study fundamental evolutionary questions, such as the link between ecology and phenotype, mechanisms maintaining genetic diversity and their putative role in speciation. Wrasses are highly diverse in ecology and morphology and harbour a variety of colour-polymorphic species. In the Mediterranean Sea, wrasses of the tribe Labrini evolved two species radiations each harbouring several species with a brown and a green morph. The colour morphs occur in complete sympatry in mosaic habitats with rocky outcrops and Neptune grass patches. Morph-specific differences had not been characterized yet and the evolutionary forces maintaining them remained unknown. With genome-wide data for almost all Labrini species, we show that species with CPs are distributed across the phylogeny, but show evidence of hybridization. This suggests that the colour morphs are either ancient and have been lost repeatedly, that they have evolved repeatedly or have been shared via hybridization. Focusing on two polymorphic species, we find that each colour morph is more common in the microhabitat providing the best colour match and that the morphs exhibit additional behavioural and morphological differences further improving crypsis in their respective microhabitats. We find little evidence for genetic differentiation between the morphs in either species. Therefore, we propose that these colour morphs represent a multi-niche polymorphism as an adaptation to the highly heterogeneous habitat. Our study highlights how colour polymorphism (CP) can be advantageous in mosaic habitats and that Mediterranean wrasses are an ideal system to study trans-species polymorphisms, i.e. polymorphisms maintained across several species, in adaptive radiations.

The Genetic Population Structure of Lake Tanganyika's Lates Species Flock, an Endemic Radiation of Pelagic Top Predators.

Understanding genetic connectivity plays a crucial role in species conservation decisions, and genetic connectivity is an important component of modern fisheries management. In this study, we investigated the population genetics of four endemic Lates species of Lake Tanganyika (Lates stappersii, L. microlepis, L. mariae, and L. angustifrons) using reduced-representation genomic sequencing methods. We find the four species to be strongly differentiated from one another (mean interspecific FST = 0.665), with no evidence for contemporary admixture. We also find evidence for strong genetic structure within L. mariae, with the majority of individuals from the most southern sampling site forming a genetic group that is distinct from the individuals at other sampling sites. We find evidence for much weaker structure within the other three species (L. stappersii, L. microlepis, and L. angustifrons). Our ability to detect this weak structure despite small and unbalanced sample sizes and imprecise geographic sampling locations suggests the possibility for further structure undetected in our study. We call for further research into the origins of the genetic differentiation in these four species-particularly that of L. mariae-which may be important for conservation and management of this culturally and economically important clade of fishes.

The propagation of admixture-derived adaptive radiation potential.

Adaptive radiations (ARs) frequently show remarkable repeatability where single lineages undergo multiple independent episodes of AR in distant places and long-separate time points. Genetic variation generated through hybridization between distantly related lineages can promote AR. This mechanism, however, requires rare coincidence in space and time between a hybridization event and opening of ecological opportunity, because hybridization generates large genetic variation only locally and it will persist only for a short period. Hence, hybridization seems unlikely to explain recurrent AR in the same lineage. Contrary to these expectations, our evolutionary computer simulations demonstrate that admixture variation can geographically spread and persist for long periods if the hybrid population becomes separated into isolated sub-lineages. Subsequent secondary hybridization of some of these can reestablish genetic polymorphisms from the ancestral hybridization in places far from the birthplace of the hybrid clade and long after the ancestral hybridization event. Consequently, simulations revealed conditions where exceptional genetic variation, once generated through a rare hybridization event, can facilitate multiple ARs exploiting ecological opportunities available at distant points in time and space.

Genetic architecture of a key reproductive isolation trait differs between sympatric and non-sympatric sister species of Lake Victoria cichlids.

One hallmark of the East African cichlid radiations is the rapid evolution of reproductive isolation that is robust to full sympatry of many closely related species. Theory predicts that species persistence and speciation in sympatry with gene flow are facilitated if loci of large effect or physical linkage (or pleiotropy) underlie traits involved in reproductive isolation. Here, we investigate the genetic architecture of a key trait involved in behavioural isolation, male nuptial coloration, by crossing two sister species pairs of Lake Victoria cichlids of the genus Pundamilia and mapping nuptial coloration in the F2 hybrids. One is a young sympatric species pair, representative of an axis of colour motif differentiation, red-dorsum versus blue, that is highly recurrent in closely related sympatric species. The other is a species pair representative of colour motifs, red-chest versus blue, that are common in allopatric but uncommon in sympatric closely related species. We find significant quantitative trait loci (QTLs) with moderate to large effects (some overlapping) for red and yellow in the sympatric red-dorsum × blue cross, whereas we find no significant QTLs in the non-sympatric red-chest × blue cross. These findings are consistent with theory predicting that large effect loci or linkage/pleiotropy underlying mating trait differentiation could facilitate speciation and species persistence with gene flow in sympatry.

Structural genomic variation leads to genetic differentiation in Lake Tanganyika's sardines.

Identifying patterns in genetic structure and the genetic basis of ecological adaptation is a core goal of evolutionary biology and can inform the management and conservation of species that are vulnerable to population declines exacerbated by climate change. We used reduced-representation genomic sequencing methods to gain a better understanding of genetic structure among and within populations of Lake Tanganyika's two sardine species, Limnothrissa miodon and Stolothrissa tanganicae. Samples of these ecologically and economically important species were collected across the length of Lake Tanganyika, as well as from nearby Lake Kivu, where L. miodon was introduced in 1959. Our results reveal differentiation within both S. tanganicae and L. miodon that is not explained by geography. Instead, this genetic differentiation is due to the presence of large sex-specific regions in the genomes of both species, but involving different polymorphic sites in each species. Our results therefore indicate rapidly evolving XY sex determination in the two species. Additionally, we found evidence of a large chromosomal rearrangement in L. miodon, creating two homokaryotypes and one heterokaryotype. We found all karyotypes throughout Lake Tanganyika, but the frequencies vary along a north-south gradient and differ substantially in the introduced Lake Kivu population. We do not find evidence for significant isolation by distance, even over the hundreds of kilometres covered by our sampling, but we do find shallow population structure.

Movement of transposable elements contributes to cichlid diversity.

African cichlid fishes are a prime model for studying speciation mechanisms. Despite the development of extensive genomic resources, it has been difficult to determine which sources of genetic variation are responsible for cichlid phenotypic variation. One of their most variable phenotypes is visual sensitivity, with some of the largest spectral shifts among vertebrates. These shifts arise primarily from differential expression of seven cone opsin genes. By mapping expression quantitative trait loci (eQTL) in intergeneric crosses of Lake Malawi cichlids, we previously identified four causative genetic variants that correspond to indels in the promoters of either key transcription factors or an opsin gene. In this comprehensive study, we show that these indels are the result of the movement of transposable elements (TEs) that correlate with opsin expression variation across the Malawi flock. In tracking the evolutionary history of these particular indels, we found they are endemic to Lake Malawi, suggesting that these TEs are recently active and are segregating within the Malawi cichlid lineage. However, an independent indel has arisen at a similar genomic location in one locus outside of the Malawi flock. The convergence in TE movement suggests these loci are primed for TE insertion and subsequent deletions. Increased TE mobility may be associated with interspecific hybridization, which disrupts mechanisms of TE suppression. This might provide a link between cichlid hybridization and accelerated regulatory variation. Overall, our study suggests that TEs may be an important driver of key regulatory changes, facilitating rapid phenotypic change and possibly speciation in African cichlids.