Adaptive Radiation Of Cichlid Fishes Research Articles

The genetics of niche-specific behavioral tendencies in an adaptive radiation of cichlid fishes.

Behavior is critical for animal survival and reproduction, and possibly for diversification and evolutionary radiation. However, the genetics behind adaptive variation in behavior are poorly understood. In this work, we examined a fundamental and widespread behavioral trait, exploratory behavior, in one of the largest adaptive radiations on Earth, the cichlid fishes of Lake Tanganyika. By integrating quantitative behavioral data from 57 cichlid species (702 wild-caught individuals) with high-resolution ecomorphological and genomic information, we show that exploratory behavior is linked to macrohabitat niche adaptations in Tanganyikan cichlids. Furthermore, we uncovered a correlation between the genotypes at a single-nucleotide polymorphism upstream of the AMPA glutamate-receptor regulatory gene cacng5b and variation in exploratory tendency. We validated this association using behavioral predictions with a neural network approach and CRISPR-Cas9 genome editing.

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 1mg. 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.

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.

Visual opsin gene expression evolution in the adaptive radiation of cichlid fishes of Lake Tanganyika.

Tuning the visual sensory system to the ambient light is essential for survival in many animal species. This is often achieved through duplication, functional diversification, and/or differential expression of visual opsin genes. Here, we examined 753 new retinal transcriptomes from 112 species of cichlid fishes from Lake Tanganyika to unravel adaptive changes in gene expression at the macro-evolutionary and ecosystem level of one of the largest vertebrate adaptive radiations. We found that, across the radiation, all seven cone opsins-but not the rhodopsin-rank among the most differentially expressed genes in the retina, together with other vision-, circadian rhythm-, and hemoglobin-related genes. We propose two visual palettes characteristic of very shallow- and deep-water living species, respectively, and show that visual system adaptations along two major ecological axes, macro-habitat and diet, occur primarily via gene expression variation in a subset of cone opsin genes.

Genetic basis of ecologically relevant body shape variation among four genera of cichlid fishes.

Divergence in body shape is one of the most widespread and repeated patterns of morphological variation in fishes and is associated with habitat specification and swimming mechanics. Such ecological diversification is the first stage of the explosive adaptive radiation of cichlid fishes in the East African Rift Lakes. We use two hybrid crosses of cichlids (Metriaclima sp. × Aulonocara sp. and Labidochromis sp. × Labeotropheus sp., >975 animals total) to determine the genetic basis of body shape diversification that is similar to benthic-pelagic divergence across fishes. Using a series of both linear and geometric shape measurements, we identified 34 quantitative trait loci (QTL) that underlie various aspects of body shape variation. These QTL are spread throughout the genome, each explaining 3.2-8.6% of phenotypic variation, and are largely modular. Further, QTL are distinct both between these two crosses of Lake Malawi cichlids and compared to previously identified QTL for body shape in fishes such as sticklebacks. We find that body shape is controlled by many genes of small effect. In all, we find that convergent body shape phenotypes commonly observed across fish clades are most likely due to distinct genetic and molecular mechanisms.

Comparative ontogenetic and transcriptomic analyses shed light on color pattern divergence in cichlid fishes.

Stripe patterns are a striking example for a repeatedly evolved color pattern. In the African adaptive radiations of cichlid fishes, stripes evolved several times independently. Previously, it has been suggested that regulatory evolution of a single gene, agouti-related-peptide 2 (agrp2), explains the evolutionary lability of this trait. Here, using a comparative transcriptomic approach, we performed comparisons between (adult) striped and nonstriped cichlid fishes of representatives of Lake Victoria and the two major clades of Lake Malawi (mbuna and non-mbuna lineage). We identify agrp2 to be differentially expressedacross all pairwise comparisons, reaffirming its association with stripe pattern divergence. We therefore also provide evidence that agrp2 is associated with the loss of the nonstereotypic oblique stripe of Mylochromis mola. Complementary ontogenetic data give insights into the development of stripe patterns as well as vertical bar patterns that both develop postembryonically. Lastly, using the Lake Victoria species pair Haplochromis sauvagei and Pundamilia nyererei, we investigated the differences between melanic and non-melanic regions to identify additional genes that contribute to the formation of stripes. Expression differences-that most importantly also do not include agrp2-are surprisingly small. This suggests, at least in this species pair, that the stripe phenotype might be caused by a combination of more subtle transcriptomic differences or cellular changes without transcriptional correlates. In summary, our comprehensive analysis highlights the ontogenetic and adult transcriptomic differences between cichlids with different color patterns and serves as a basis for further investigation of the mechanistic underpinnings of their diversification.

Molecular evolution and depth-related adaptations of rhodopsin in the adaptive radiation of cichlid fishes in Lake Tanganyika.

The visual sensory system is essential for animals to perceive their environment and is thus under strong selection. In aquatic environments, light intensity and spectrum differ primarily along a depth gradient. Rhodopsin (RH1) is the only opsin responsible for dim‐light vision in vertebrates and has been shown to evolve in response to the respective light conditions, including along a water depth gradient in fishes. In this study, we examined the diversity and sequence evolution of RH1 in virtually the entire adaptive radiation of cichlid fishes in Lake Tanganyika, focusing on adaptations to the environmental light with respect to depth. We show that Tanganyikan cichlid genomes contain a single copy of RH1. The 76 variable amino acid sites detected in RH1 across the radiation were not uniformly distributed along the protein sequence, and 31 of these variable sites show signals of positive selection. Moreover, the amino acid substitutions at 15 positively selected sites appeared to be depth‐related, including three key tuning sites that directly mediate shifts in the peak spectral sensitivity, one site involved in protein stability and 11 sites that may be functionally important on the basis of their physicochemical properties. Among the strongest candidate sites for deep‐water adaptations are two known key tuning sites (positions 292 and 299) and three newly identified variable sites (37, 104 and 290). Our study, which is the first comprehensive analysis of RH1 evolution in a massive adaptive radiation of cichlid fishes, provides novel insights into the evolution of RH1 in a freshwater environment.

Tracing evolutionary decoupling of oral and pharyngeal jaws in cichlid fishes.

Evolutionary innovations can facilitate diversification if the novel trait enables a lineage to exploit new niches or by expanding character space. The elaborate pharyngeal jaw apparatus of cichlid fishes is often referred to as an evolutionary “key innovation” that has promoted the spectacular adaptive radiations in these fishes. This goes back to the idea that the structural and functional independence of the oral and pharyngeal jaws for food capturing and food processing, respectively, permitted each jaw type to follow independent evolutionary trajectories. This “evolutionary decoupling” is thought to have facilitated novel trait combinations and, hence, ecological specialization, ultimately allowing more species to coexist in sympatry. Here, we test the hypotheses of evolutionary decoupling of the oral and pharyngeal jaws in the massive adaptive radiation of cichlid fishes in African Lake Tanganyika. Based on phylogenetic comparative analyses of oral jaw morphology and lower pharyngeal jaw shape across most of the ∼240 cichlid species occurring in that lake, we show that the two jaws evolved coupled along the main axes of morphological variation, yet most other components of these trait complexes evolved largely independently over the course of the radiation. Further, we find limited correlations between the two jaws in both overall divergence and evolutionary rates. Moreover, we show that the two jaws were evolutionary decoupled at a late stage of the radiation, suggesting that decoupling contributed to micro‐niche partitioning and the associated rapidly increasing trophic diversity during this phase.

Comparative scale morphology in the adaptive radiation of cichlid fishes (Perciformes: Cichlidae) from Lake Tanganyika

Abstract The morphology of fish scales has been investigated for > 200 years, but research on evolutionary patterns of scale morphology is scarce. Here, we study scale morphology and its evolution in the adaptive radiation of cichlid fishes from Lake Tanganyika, which are known for their exceptional diversity in habitat use, feeding ecology and morphology. Based on a geometric morphometric approach on eight scales per specimen (covering different body regions), we quantify scale types and morphology across nearly all ~240 species of the cichlid adaptive radiation in Lake Tanganyika. We first show that scale type, shape and ctenii coverage vary along the body, which is probably attributable to adaptations to different functional demands on the respective scales. Our comparative analyses reveal that flank scale size is tightly linked to phylogeny, whereas scale shape and ctenii coverage can be explained only in part by phylogenetic history and/or our proxy for ecology (stable isotopes and body shape), suggesting an additional adaptive component. We also show that our measured scale characteristics can help to assign an individual scale to a taxonomic group or ecotype. Thus, our data may serve as a valuable resource for taxonomic studies and to interpret fossil finds.

Drivers and dynamics of a massive adaptive radiation in cichlid fishes.

Adaptive radiation is the likely source of much of the ecological and morphological diversity of life1-4. How adaptive radiations proceed and what determines their extent remains unclear in most cases1,4. Here we report the in-depth examination of the spectacular adaptive radiation of cichlid fishes in Lake Tanganyika. On the basis of whole-genome phylogenetic analyses, multivariate morphological measurements of three ecologically relevant trait complexes (body shape, upper oral jaw morphology and lower pharyngeal jaw shape), scoring of pigmentation patterns and approximations of the ecology of nearly all of theapproximately 240 cichlid species endemic to Lake Tanganyika, we show that the radiation occurred within the confines of the lake and that morphological diversification proceeded in consecutive trait-specific pulses of rapid morphospace expansion. We provide empirical support for two theoretical predictions of how adaptive radiations proceed, the 'early-burst' scenario1,5 (for body shape) and the stages model1,6,7 (for all traits investigated). Through the analysis of two genomes per species and by taking advantage of the uneven distribution of species in subclades of the radiation, we further show that species richness scales positively with per-individual heterozygosity, but is not correlated with transposable element content, number of gene duplications or genome-wide levels of selection in coding sequences.

Developmental and Cellular Basis of Vertical Bar Color Patterns in the East African Cichlid Fish Haplochromis latifasciatus.

The East African adaptive radiations of cichlid fishes are renowned for their diversity in coloration. Yet, the developmental basis of pigment pattern formation remains largely unknown. One of the most common melanic patterns in cichlid fishes are vertical bar patterns. Here we describe the ontogeny of this conspicuous pattern in the Lake Kyoga species Haplochromis latifasciatus. Beginning with the larval stages we tracked the formation of this stereotypic color pattern and discovered that its macroscopic appearance is largely explained by an increase in melanophore density and accumulation of melanin during the first 3 weeks post-fertilization. The embryonal analysis is complemented with cytological quantifications of pigment cells in adult scales and the dermis beneath the scales. In adults, melanic bars are characterized by a two to threefold higher density of melanophores than in the intervening yellow interbars. We found no strong support for differences in other pigment cell types such as xanthophores. Quantitative PCRs for twelve known pigmentation genes showed that expression of melanin synthesis genes tyr and tyrp1a is increased five to sixfold in melanic bars, while xanthophore and iridophore marker genes are not differentially expressed. In summary, we provide novel insights on how vertical bars, one of the most widespread vertebrate color patterns, are formed through dynamic control of melanophore density, melanin synthesis and melanosome dispersal.

Ancestral Hybridization Facilitated Species Diversification in the Lake Malawi Cichlid Fish Adaptive Radiation.

The adaptive radiation of cichlid fishes in East African Lake Malawi encompasses over 500 species that are believed to have evolved within the last 800,000 years from a common founder population. It has been proposed that hybridization between ancestral lineages can provide the genetic raw material to fuel such exceptionally high diversification rates, and evidence for this has recently been presented for the Lake Victoria region cichlid superflock. Here, we report that Lake Malawi cichlid genomes also show evidence of hybridization between two lineages that split 3–4 Ma, today represented by Lake Victoria cichlids and the riverine Astatotilapia sp. “ruaha blue.” The two ancestries in Malawi cichlid genomes are present in large blocks of several kilobases, but there is little variation in this pattern between Malawi cichlid species, suggesting that the large-scale mosaic structure of the genomes was largely established prior to the radiation. Nevertheless, tens of thousands of polymorphic variants apparently derived from the hybridization are interspersed in the genomes. These loci show a striking excess of differentiation across ecological subgroups in the Lake Malawi cichlid assemblage, and parental alleles sort differentially into benthic and pelagic Malawi cichlid lineages, consistent with strong differential selection on these loci during species divergence. Furthermore, these loci are enriched for genes involved in immune response and vision, including opsin genes previously identified as important for speciation. Our results reinforce the role of ancestral hybridization in explosive diversification by demonstrating its significance in one of the largest recent vertebrate adaptive radiations.

Island- and lake-like parallel adaptive radiations replicated in rivers.

Parallel adaptive radiations have arisen following the colonization of islands by lizards and lakes by fishes. In these classic examples, parallel adaptive radiation is a response to the ecological opportunities afforded by the colonization of novel ecosystems and similar adaptive landscapes that favour the evolution of similar suites of ecomorphs, despite independent evolutionary histories. Here, we demonstrate that parallel adaptive radiations of cichlid fishes arose in South American rivers. Speciation-assembled communities of pike cichlids (Crenicichla) have independently diversified into similar suites of novel ecomorphs in the Uruguay and Paraná Rivers, including crevice feeders, periphyton grazers and molluscivores. There were bursts in phenotypic evolution associated with the colonization of each river and the subsequent expansion of morphospace following the evolution of the ecomorphs. These riverine clades demonstrate that characteristics emblematic of textbook parallel adaptive radiations of island- and lake-dwelling assemblages are feasible evolutionary outcomes even in labile ecosystems such as rivers.

Ecological opportunity alters the timing and shape of adaptive radiation.

The uneven distribution of diversity is a conspicuous phenomenon across the tree of life. Ecological opportunity is a prominent catalyst of adaptive radiation and therefore may alter patterns of diversification. We evaluated the distribution of shifts in diversification rates across the cichlid phylogeny and the distribution of major clades across phylogenetic space. We also tested if ecological opportunity influenced these patterns. Colonization-associated ecological opportunity altered the tempo and mode of diversification during the adaptive radiation of cichlid fishes. Clades that arose following colonization events diversified faster than other clades. Speciation rate shifts were nonrandomly distributed across the phylogeny such that they were disproportionally concentrated around nodes that corresponded with colonization events (i.e., of continents, river basins, or lakes). Young clades tend to expand faster than older clades; however, colonization-associated ecological opportunity accentuated this pattern. There was an interaction between clade age and ecological opportunity that explained the trajectory of clades through phylogenetic space over time. Our results indicate that ecological opportunities afforded by continental and ecosystem-scale colonization events explain the dramatic speciation rate heterogeneity and phylogenetic imbalance that arose during the evolutionary history of cichlid fishes.

Parasite escape through trophic specialization in a species flock.

Adaptive radiation occurs when species diversify rapidly to occupy an array of ecological niches. As opportunities for parasite infection and transmission may greatly vary among these niches, adaptive radiation is expected to be associated with a turnover of the parasite community. As major agents of natural and sexual selection, parasites may play a central role in host diversification. The study of parasite turnover may thus be of general relevance and could significantly improve our understanding of adaptive radiation. In this study, we examined the parasite faunas of eleven species belonging to the tribe Tropheini, one of several adaptive radiations of cichlid fishes in Lake Tanganyika. The most parsimonious ancestral foraging strategy among the Tropheini is relatively unselective substrate browsing of aufwuchs. Several lineages evolved more specialized foraging strategies, such as selective combing of microscopic diatoms or picking of macro-invertebrates. We found that representatives of these specialized lineages bear reduced infection with food-web-transmitted acanthocephalan helminths, but not with parasites with a direct life cycle. Possibly, the evolution of selective foraging strategies entailed reduced ingestion of intermediate invertebrate hosts of acanthocephalans. We conclude that some species belonging to the Tropheini virtually escape acanthocephalan infection as a by-product of trophic specialization.

Depth segregation and diet disparity revealed by stable isotope analyses in sympatric herbivorous cichlids in Lake Tanganyika.

BackgroundLake Tanganyika in the African Great Rift Valley is known as a site of adaptive radiation in cichlid fishes. Diverse herbivorous fishes coexist on a rocky littoral of the lake. Herbivorous cichlids have acquired multiple feeding ecomorphs, including grazer, browser, scraper, and scooper, and are segregated by dietary niche. Within each ecomorph, however, multiple species apparently coexist sympatrically on a rocky slope. Previous observations of their behavior show that these cichlid species inhabit discrete depths separated by only a few meters. In this paper, using carbon (C) and nitrogen (N) stable isotope ratios as markers, we followed the nutritional uptake of cichlid fishes from periphyton in their feeding territories at various depths.Resultsδ15N of fish muscles varied among cichlid ecomorphs; this was significantly lower in grazers than in browsers and scoopers, although δ15N levels in periphyton within territories did not differ among territorial species. This suggests that grazers depend more directly on primary production of periphyton, while others ingest animal matter from higher trophic levels. With respect to δ13C, only plankton eaters exhibited lower values, suggesting that these fishes depend on production of phytoplankton, while the others depend on production of periphyton. Irrespective of cichlid ecomorph, δ13C of periphyton correlated significantly with habitat depth, and decreased as habitat depth became deeper. δ13C in territorial fish muscles was significantly related to that of periphyton within their territories, regardless of cichlid ecomorph, which suggests that these herbivorous cichlids depend on primary production of periphyton within their territories.ConclusionsCarbon and nitrogen stable isotope ratios varied among ecomorphs and among cichlid species in the same ecomorphs sympatrically inhabiting a littoral area of Lake Tanganyika, suggesting that these cichlids are segregated by nutrient source due to varying dependency on periphyton in different ecomorphs (especially between grazers and browsers), and due to segregation of species of the same ecomorph by feeding depth, grazers and browsers in particular.Electronic supplementary materialThe online version of this article (doi:10.1186/s40851-015-0016-1) contains supplementary material, which is available to authorized users.

What big lips are good for: on the adaptive function of repeatedly evolved hypertrophied lips of cichlid fishes

Linking phenotypic traits to an adaptive ecological function is a major goal of evolutionary biology. However, this task is challenging and has been accomplished in only a handful of species and ecological model systems. The repeatedly evolved adaptive radiations of cichlid fishes are composed of an enormously diverse set of species that differ in trophic morphology, body shape, coloration, and behaviour. Ecological guilds of species with conspicuously hypertrophied lips have evolved in parallel in all major cichlid radiations and are characterized by large lips and pointed and narrow heads. In the present study, we experimentally tested the adaptive significance of this set of conspicuous traits by comparing the success of hypertrophied-lipped and closely-related thin-lipped endemic Lake Victoria cichlids in a novel foraging assay. The hypertrophied-lipped species (Haplochromis chilotes) was clearly more successful in exploiting food resources from narrow crevices and the observed difference in foraging success increased more at narrower angles. Furthermore, pronounced differences in exploratory behaviour between the species suggest that the evolution of hypertrophied-lipped species involved the co-evolution of a suite of traits that include foraging behaviour. The repeated evolution of hypertrophied-lip morphology in conjunction with a narrow and pointed head shape in cichlids represents an evolutionary innovation that facilitates foraging in rocky crevices, thus allowing access to a novel niche. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115, 448–455.

Testing the stages model in the adaptive radiation of cichlid fishes in East African Lake Tanganyika.

Adaptive radiation (AR) is a key process in the origin of organismal diversity. However, the evolution of trait disparity in connection with ecological specialization is still poorly understood. Available models for vertebrate ARs predict that diversification occurs in the form of temporal stages driven by different selective forces. Here, we investigate the AR of cichlid fishes in East African Lake Tanganyika and use macroevolutionary model fitting to evaluate whether diversification happened in temporal stages. Six trait complexes, for which we also provide evidence of their adaptiveness, are analysed with comparative methods: body shape, pharyngeal jaw shape, gill raker traits, gut length, brain weight and body coloration. Overall, we do not find strong evidence for the 'stages model' of AR. However, our results suggest that trophic traits diversify earlier than traits implicated in macrohabitat adaptation and that sexual communication traits (i.e. coloration) diversify late in the radiation.

Turnover and accumulation of genetic diversity across large time-scale cycles of isolation and connection of populations.

Major climatic and geological events but also population history (secondary contacts) have generated cycles of population isolation and connection of long and short periods. Recent empirical and theoretical studies suggest that fast evolutionary processes might be triggered by such events, as commonly illustrated in ecology by the adaptive radiation of cichlid fishes (isolation and reconnection of lakes and watersheds) and in epidemiology by the fast adaptation of the influenza virus (isolation and reconnection in hosts). We test whether cyclic population isolation and connection provide the raw material (standing genetic variation) for species evolution and diversification. Our analytical results demonstrate that population isolation and connection can provide, to populations, a high excess of genetic diversity compared with what is expected at equilibrium. This excess is either cyclic (high allele turnover) or cumulates with time depending on the duration of the isolation and the connection periods and the mutation rate. We show that diversification rates of animal clades are associated with specific periods of climatic cycles in the Quaternary. We finally discuss the importance of our results for macroevolutionary patterns and for the inference of population history from genomic data.

Convergent Evolution within an Adaptive Radiation of Cichlid Fishes

The recurrent evolution of convergent forms is a widespread phenomenon in adaptive radiations (e.g., [1-9]). For example, similar ecotypes of anoles lizards have evolved on different islands of the Caribbean, benthic-limnetic species pairs of stickleback fish emerged repeatedly in postglacial lakes, equivalent sets of spider ecomorphs have arisen on Hawaiian islands, and a whole set of convergent species pairs of cichlid fishes evolved in East African Lakes Malawi and Tanganyika. In all these cases, convergent phenotypes originated in geographic isolation from each other. Recent theoretical models, however, predict that convergence should be common within species-rich communities, such as species assemblages resulting from adaptive radiations. Here, we present the most extensive quantitative analysis to date of an adaptive radiation of cichlid fishes, discovering multiple instances of convergence in body and trophic morphology. Moreover, we show that convergent morphologies are associated with adaptations to specific habitats and resources and that Lake Tanganyika's cichlid communities are characterized by the sympatric occurrence of convergent forms. This prevalent coexistence of distantly related yet ecomorphologically similar species offers an explanation for the greatly elevated species numbers in cichlid species flocks.