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 the approximately 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.

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.

Contrasting signatures of genomic divergence during sympatric speciation.

The transition from 'well-marked varieties' of a single species into 'well-defined species'-especially in the absence of geographic barriers to gene flow (sympatric speciation)-has puzzled evolutionary biologists ever since Darwin1,2. Gene flow counteracts the buildup of genome-wide differentiation, which is a hallmark of speciation and increases the likelihood of the evolution of irreversible reproductive barriers (incompatibilities) that complete the speciation process3. Theory predicts that the genetic architecture of divergently selected traits can influence whether sympatric speciation occurs4, but empirical tests of this theory are scant because comprehensive data are difficult to collect and synthesize across species, owing to their unique biologies and evolutionary histories5. Here, within a young species complex of neotropical cichlid fishes (Amphilophus spp.), we analysed genomic divergence among populations and species. By generating a new genome assembly and re-sequencing 453 genomes, we uncovered the genetic architecture of traits that have been suggested to be important for divergence. Species that differ in monogenic or oligogenic traits that affect ecological performance and/or mate choice show remarkably localized genomic differentiation. By contrast, differentiation among species that have diverged in polygenic traits is genomically widespread and much higher overall, consistent with the evolution of effective and stable genome-wide barriers to gene flow. Thus, we conclude that simple trait architectures are not always as conducive to speciation with gene flow as previously suggested, whereas polygenic architectures can promote rapid and stable speciation in sympatry.

Severe Bottleneck Impacted the Genomic Structure of Egg-Eating Cichlids in Lake Victoria.

Within 15,000 years, the explosive adaptive radiation of haplochromine cichlids in Lake Victoria, East Africa, generated 500 endemic species. In the 1980s, the upsurge of Nile perch, a carnivorous fish artificially introduced to the lake, drove the extinction of more than 200 endemic cichlids. The Nile perch predation particularly harmed piscivorous cichlids, including paedophages, cichlids eat eggs and fries, which is an example of the unique trophic adaptation seen in African cichlids. Here, aiming to investigate past demographic events possibly triggered by the invasion of Nile perch and the subsequent impacts on the genetic structure of cichlids, we conducted large-scale comparative genomics. We discovered evidence of recent bottleneck events in 4 species, including 2 paedophages, which began during the 1970s to 1980s, and population size rebounded during the 1990s to 2000s. The timing of the bottleneck corresponded to the historical records of endemic haplochromines" disappearance and later resurgence, which is likely associated with the introduction of Nile perch by commercial demand to Lake Victoria in the 1950s. Interestingly, among the 4 species that likely experienced bottleneck, Haplochromis sp. "matumbi hunter," a paedophagous cichlid, showed the most severe bottleneck signatures. The components of shared ancestry inferred by ADMIXTURE suggested a high genetic differentiation between matumbi hunter and other species. In contrast, our phylogenetic analyses highly supported the monophyly of the 5 paedophages, consistent with the results of previous studies. We conclude that high genetic differentiation of matumbi hunter occurred due to the loss of shared genetic components among haplochromines in Lake Victoria caused by the recent severe bottleneck.

Polygenic sex determination produces modular sex polymorphism in an African cichlid fish.

For many vertebrates, a single genetic locus initiates a cascade of developmental sex differences in the gonad and throughout the organism, resulting in adults with two phenotypically distinct sexes. Species with polygenic sex determination (PSD) have multiple interacting sex determination alleles segregating within a single species, allowing for more than two genotypic sexes and scenarios where sex genotype at a given locus can be decoupled from gonadal sex. Here we investigate the effects of PSD on secondary sexual characteristics in the cichlid fish Metriaclima mbenjii, where one female (W) and one male (Y) sex determination allele interact to produce siblings with four possible sex classes: ZZXX females, ZWXX females, ZWXY females, and ZZXY males. We find that PSD in M. mbenjii produces an interplay of sex linkage and sex limitation resulting in modular variation in morphological and behavioral traits. Further, the evolution or introgression of a newly acquired sex determiner creates additional axes of phenotypic variation for varied traits, including genital morphology, craniofacial morphology, gastrointestinal morphology, and home tank behaviors. In contrast to single-locus sex determination, which broadly results in sexual dimorphism, polygenic sex determination can induce higher-order sexual polymorphism. The modularity of secondary sexual characteristics produced by PSD provides context for understanding the evolutionary causes and consequences of maintenance, gain, or loss of sex determination alleles in populations.

Genetic diversity and population structure of farmed and wild Nile tilapia (Oreochromis niloticus) in Uganda: The potential for aquaculture selection and breeding programs.

Nile tilapia is one of the most important aquaculture species globally, providing high-quality animal protein for human nutrition and a source of income to sustain the livelihoods of many people in low- and middle-income countries. This species is native to Africa and nowadays farmed throughout the world. However, the genetic makeup of its native populations remains poorly characterized. Additionally, there has been important introgression and movement of farmed (as well as wild) strains connected to tilapia aquaculture in Africa, yet the relationship between wild and farmed populations is unknown in most of the continent. Genetic characterization of the species in Africa has the potential to support the conservation of the species as well as supporting selective breeding to improve the indigenous strains for sustainable and profitable aquaculture production. In the current study, a total of 382 fish were used to investigate the genetic structure, diversity, and ancestry within and between Ugandan Nile tilapia populations from three major lakes including Lake Albert (L. Albert), Lake Kyoga (L. Kyoga) and Lake Victoria (L. Victoria), and 10 hatchery farms located in the catchment regions of these lakes. Our results showed clear genetic structure of the fish sourced from the lakes, with L. Kyoga and L. Albert populations showing higher genetic similarity. We also observed noticeable genetic structure among farmed populations, with most of them being genetically similar to L. Albert and L. Kyoga fish. Admixture results showed a higher (2.55-52.75%) contribution of L. Albert / L. Kyoga stocks to Uganda's farmed fish than the stock from L. Victoria (2.12-28.02%). We observed relatively high genetic diversity across both wild and farmed populations, but some farms had sizable numbers of highly inbred fish, raising concerns about management practices. In addition, we identified a genomic region on chromosome 5, harbouring the key innate immune gene BPI and the key growth gene GHRH, putatively under selection in the Ugandan Nile tilapia population. This region overlaps with the genomic region previously identified to be associated with growth rate in farmed Nile tilapia.

Integrative analysis of miRNA-mRNA expression in the brain during high temperature-induced masculinization of female Nile tilapia (Oreochromis niloticus).

Temperature is one of the most important non-genetic sex differentiation factors for fish. The technique of high temperature-induced sex reversal is commonly used in Nile tilapia (Oreochromis niloticus) culture, although the molecular regulatory mechanisms involved in this process remain unclear. The brain is an essential organ for the regulation of neural signals involved in germ cell differentiation and gonad development. To investigate the regulatory roles of miRNAs-mRNAs in the conversion of female to male Nile tilapia gender under high-temperature stress, we compared RNA-Seq data from brain tissues between a control group (28 °C) and a high temperature-treated group (36 °C). The result showed that a total of 123,432,984 miRNA valid reads, 288,202,524 mRNA clean reads, 1128 miRNAs, and 32,918 mRNAs were obtained. Among them, there were 222 significant differentially expressed miRNAs (DE miRNAs) and 810 differentially expressed mRNAs (DE mRNAs) between the two groups. Eight DE miRNAs and eight DE mRNAs were randomly selected, and their expression patterns were validated by qRT-PCR. The miRNA-mRNA co-expression network demonstrated that 40 DE miRNAs targeted 136 protein-coding genes. Functional enrichment analysis demonstrated that these genes were involved in several gonadal differentiation pathways, including the oocyte meiosis signaling pathway, progesterone-mediated oocyte maturation signaling pathway, cell cycle signaling pathway and GnRH signaling pathway. Then, an interaction network was constructed for 8 miRNAs (mir-137-5p, let-7d, mir-1388-5p, mir-124-4-5p, mir-1306, mir-99, mir-130b and mir-21) and 10 mRNAs (smc1al, itpr2, mapk1, ints8, cpeb1b, bub1, fbxo5, mmp14b, cdk1 and hrasb) involved in the oocyte meiosis signaling pathway. These findings provide novel information about the mechanisms underlying miRNA-mediated sex reversal in female Nile tilapia.

Study on the osmotic response and function of myo-inositol oxygenase in euryhaline fish nile tilapia (Oreochromis niloticus).

To understand the role of myo-inositol oxygenase (miox) in the osmotic regulation of Nile tilapia, its expression was analyzed in various tissues. The results showed that the expression of miox gene was highest in the kidney, followed by the liver, and was significantly upregulated in the kidney and liver under 1 h hyperosmotic stress. The relative luminescence efficiency of the miox gene transcription starting site (-4,617 to +312 bp) under hyperosmotic stress was measured. Two fragments (-1,640/-1,619 and -620/-599) could induce the luminescence activity. Moreover, the -1,640/-1,619 and -620/-599 responded to hyperosmotic stress and high-glucose stimulation by base mutation, suggesting that osmotic and carbohydrate response elements may exist in this region. Finally, the salinity tolerance of Nile tilapia was significantly reduced after the knocking down of miox gene. The accumulation of myo-inositol was affected, and the expression of enzymes in glucose metabolism was significantly reduced after the miox gene was knocked down. Furthermore, hyperosmotic stress can cause oxidative stress, and MIOX may help maintain the cell redox balance under hyperosmotic stress. In summary, MIOX is essential in osmotic regulation to enhance the salinity tolerance of Nile tilapia by affecting myo-inositol accumulation, glucose metabolism, and antioxidant performance.NEW & NOTEWORTHY Myo-inositol oxygenase (MIOX) is the rate-limiting enzyme that catalyzes the first step of MI metabolism and determines MI content in aquatic animals. To understand the role of miox in the osmotic regulation of Nile tilapia, we analyzed its expression in different tissues and its function under hyperosmotic stress. This study showed that miox is essential in osmotic regulation to enhance the salinity tolerance of Nile tilapia by affecting myo-inositol accumulation, glucose metabolism, and antioxidant performance.

Developmental plasticity and variability in the formation of egg-spots, a pigmentation ornament in the cichlid Astatotilapia calliptera.

Vertebrate pigmentation patterns are highly diverse, yet we have a limited understanding of how evolutionary changes to genetic, cellular, and developmental mechanisms generate variation. To address this, we examine the formation of a sexually-selected male ornament exhibiting inter- and intraspecific variation, the egg-spot pattern, consisting of circular yellow-orange markings on the male anal fins of haplochromine cichlid fishes. We focus on Astatotilapia calliptera, the ancestor-type species of the Malawi cichlid adaptive radiation of over 850 species. We identify a key role for iridophores in initializing egg-spot aggregations composed of iridophore-xanthophore associations. Despite adult sexual dimorphism, aggregations initially form in both males and females, with development only diverging between the sexes at later stages. Unexpectedly, we found that the timing of egg-spot initialization is plastic. The earlier individuals are socially isolated, the earlier the aggregations form, with iridophores being the cell type that responds to changes to the social environment. Furthermore, we observe apparent competitive interactions between adjacent egg-spot aggregations, which strongly suggests that egg-spot patterning results mostly from cell-autonomous cellular interactions. Together, these results demonstrate that A. calliptera egg-spot development is an exciting model for investigating pigment pattern formation at the cellular level in a system with developmental plasticity, sexual dimorphism, and intraspecific variation. As A. calliptera represents the ancestral bauplan for egg-spots, these findings provide a baseline for informed comparisons across the incredibly diverse Malawi cichlid radiation.

Developmental and environmental plasticity in opsin gene expression in Lake Victoria cichlid fish.

In many organisms, sensory abilities develop and evolve according to the changing demands of navigating, foraging, and communication across different environments and life stages. Teleost fish inhabit heterogeneous light environments and exhibit a large diversity in visual system properties among species. Cichlids are a classic example of this diversity; visual system variation is generated by different tuning mechanisms that involve both genetic factors and phenotypic plasticity. Here, we document the developmental progression of visual pigment gene expression in Lake Victoria cichlids and test if these patterns are influenced by variation in light conditions. We reared two sister species of Pundamilia to adulthood in two distinct visual conditions that resemble the light environments that they naturally inhabit in Lake Victoria. We also included interspecific first-generation hybrids. We focused on the four opsins that are expressed in Pundamilia adults (using real-time quantitative polymerase chain reaction (RT-qPCR)) (SWS2B, SWS2A, RH2A, and LWS) at 17 time points. We find that opsin expression profiles progress from shorter-wavelength sensitive opsins to longer-wavelength sensitive opsins with increasing age, in both species and their hybrids. The developmental trajectories of opsin expression also responded plastically to the visual conditions. Developmental and environmental plasticity in opsin expression may provide an important stepping stone in the evolution of cichlid visual system diversity.

Repeated Divergence in Opsin Gene Expression Mirrors Photic Habitat Changes in Rapidly Evolving Crater Lake Cichlid Fishes.

AbstractSelection pressures differ along environmental gradients, and traits tightly linked to fitness (e.g., the visual system) are expected to track such variation. Along gradients, adaptation to local conditions might be due to heritable and nonheritable environmentally induced variation. Disentangling these sources of phenotypic variation requires studying closely related populations in nature and in the laboratory. The Nicaraguan lakes represent an environmental gradient in photic conditions from clear crater lakes to very turbid great lakes. From two old, turbid great lakes, Midas cichlid fish (Amphilophus cf. citrinellus) independently colonized seven isolated crater lakes of varying light conditions, resulting in a small adaptive radiation. We estimated variation in visual sensitivities along this photic gradient by measuring cone opsin gene expression among lake populations. Visual sensitivities observed in all seven derived crater lake populations shifted predictably in direction and magnitude, repeatedly mirroring changes in photic conditions. Comparing wild-caught and laboratory-reared fish revealed that 48% of this phenotypic variation is genetically determined and evolved rapidly. Decreasing intrapopulation variation as environments become spectrally narrower suggests that different selective landscapes operate along the gradient. We conclude that the power to predict phenotypic evolution along gradients depends on both the magnitude of environmental change and the selective landscape shape.

Germline sexual fate is determined by the antagonistic action of dmrt1 and foxl3/foxl2 in tilapia.

Germline sexual fate has long been believed to be determined by the somatic environment, but this idea is challenged by recent studies of foxl3 mutants in medaka. Here, we demonstrate that the sexual fate of tilapia germline is determined by the antagonistic interaction of dmrt1 and foxl3, which are transcriptionally repressed in male and female germ cells, respectively. Loss of dmrt1 rescued the germ cell sex reversal in foxl3Δ7/Δ7 XX fish, and loss of foxl3 partially rescued germ cell sex reversal but not somatic cell fate in dmrt1Δ5/Δ5 XY fish. Interestingly, germ cells lost sexual plasticity in dmrt1Δ5/Δ5 XY and foxl3Δ7/Δ7 XX single mutants, as aromatase inhibitor (AI) and estrogen treatment failed to rescue the respective phenotypes. However, recovery of germ cell sexual plasticity was observed in dmrt1/foxl3 double mutants. Importantly, mutation of somatic cell-specific foxl2 resulted in testicular development in foxl3Δ7/Δ7 or dmrt1Δ5/Δ5 mutants. Our findings demonstrate that sexual plasticity of germ cells relies on the presence of both dmrt1 and foxl3. The existence of dmrt1 and foxl3 allows environmental factors to influence the sex fate decision in vertebrates.

Foraging-induced craniofacial plasticity is associated with an early, robust and dynamic transcriptional response.

Phenotypic plasticity is the ability of a single genotype to vary its phenotype in response to the environment. Plasticity of the skeletal system in response to mechanical input is widely studied, but the timing of its transcriptional regulation is not well understood. Here, we used the cichlid feeding apparatus to examine the transcriptional dynamics of skeletal plasticity over time. Using three closely related species that vary in their ability to remodel bone and a panel of 11 genes, including well-studied skeletal differentiation markers and newly characterized environmentally sensitive genes, we examined plasticity at one, two, four and eight weeks following the onset of alternate foraging challenges. We found that the plastic species exhibited environment-specific bursts in gene expression beginning at one week, followed by a sharp decline in levels, while the species with more limited plasticity exhibited consistently low levels of gene expression. This trend held across nearly all genes, suggesting that it is a hallmark of the larger plasticity regulatory network. We conclude that plasticity of the cichlid feeding apparatus is not the result of slowly accumulating gene expression difference over time, but rather is stimulated by early bursts of environment-specific gene expression followed by a return to homeostatic levels.

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.

Exon-based Phylogenomics and the Relationships of African Cichlid Fishes: Tackling the Challenges of Reconstructing Phylogenies with Repeated Rapid Radiations.

African cichlids (subfamily: Pseudocrenilabrinae) are among the most diverse vertebrates, and their propensity for repeated rapid radiation has made them a celebrated model system in evolutionary research. Nonetheless, despite numerous studies, phylogenetic uncertainty persists, and riverine lineages remain comparatively underrepresented in higher-level phylogenetic studies. Heterogeneous gene histories resulting from incomplete lineage sorting (ILS) and hybridization are likely sources of uncertainty, especially during episodes of rapid speciation. We investigate the relationships of Pseudocrenilabrinae and its close relatives while accounting for multiple sources of genetic discordance using species tree and hybrid network analyses with hundreds of single-copy exons. We improve sequence recovery for distant relatives, thereby extending the taxonomic reach of our probes, with a hybrid reference guided/de novo assembly approach. Our analyses provide robust hypotheses for most higher-level relationships and reveal widespread gene heterogeneity, including in riverine taxa. ILS and past hybridization are identified as the sources of genetic discordance in different lineages. Sampling of various Blenniiformes (formerly Ovalentaria) adds strong phylogenomic support for convict blennies (Pholidichthyidae) as sister to Cichlidae and points to other potentially useful protein-coding markers across the order. A reliable phylogeny with representatives from diverse environments will support ongoing taxonomic and comparative evolutionary research in the cichlid model system. [African cichlids; Blenniiformes; Gene tree heterogeneity; Hybrid assembly; Phylogenetic network; Pseudocrenilabrinae; Species tree.].

Rapid Parallel Morphological and Mechanical Diversification of South American Pike Cichlids (Crenicichla).

Explosive bouts of diversification are one of the most conspicuous features of the tree of life. When such bursts are repeated in similar environments, it suggests some degree of predictability in the evolutionary process. We assess parallel adaptive radiation of South American pike cichlids (Crenicichla) using phylogenomics and phylogenetic comparative methods. We find that species flocks in the Uruguay and Iguazú River basins rapidly diversified into the same set of ecomorphs that reflect feeding ecology. Both adaptive radiations involve expansion of functional morphology, resulting in unique jaw phenotypes. Yet, form and function were decoupled such that most ecomorphs share similar mechanical properties of the jaws (i.e., jaw motion during a feeding strike). Prey mobility explained 6- to 9-fold differences in the rate of morphological evolution but had no effect on the rate of mechanical evolution. We find no evidence of gene flow between species flocks or with surrounding coastal lineages that may explain their rapid diversification. When compared with cichlids of the East African Great Lakes and other prominent adaptive radiations, pike cichlids share many themes, including the rapid expansion of phenotypic diversity, specialization along the benthic-to-pelagic habitat and soft-to-hard prey axes, and the evolution of conspicuous functional innovations. Yet, decoupled evolution of form and function and the absence of hybridization as a catalyzing force are departures from patterns observed in other adaptive radiations. Many-to-one mapping of morphology to mechanical properties is a mechanism by which pike cichlids attain a diversity of feeding ecologies while avoiding exacerbating underlying mechanical trade-offs. [Adaptive radiation; ecological opportunity; feeding kinematics; functional trade-off; hybridization; introgression.].

Functional Trade-Offs Asymmetrically Promote Phenotypic Evolution.

Trade-offs are thought to bias evolution and are core features of many anatomical systems. Therefore, trade-offs may have far-reaching macroevolutionary consequences, including patterns of morphological, functional, and ecological diversity. Jaws, like many complex anatomical systems, are comprised of elements involved in biomechanical trade-offs. We test the impact of a core mechanical trade-off, the transmission of velocity versus force (i.e., mechanical advantage), on rates of jaw evolution in Neotropical cichlids. Across 130 species representing a wide array of feeding ecologies, we find that the velocity-force trade-off impacts the evolution of the surrounding jaw system. Specifically, rates of jaw evolution are faster at functional extremes than in more functionally intermediate or unspecialized jaws. Yet, surprisingly, the effect on jaw evolution is uneven across the extremes of the velocity-force continuum. Rates of jaw evolution are 4- to 10-fold faster in velocity-modified jaws, whereas force-modified jaws are 7- to 18-fold faster, compared to unspecialized jaws, depending on the extent of specialization. Further, we find that a more extreme mechanical trade-off resulted in faster rates of jaw evolution. The velocity-force trade-off reflects a gradient from specialization on capture-intensive (e.g., evasive or buried) to processing-intensive prey (e.g., attached or shelled), respectively. The velocity extreme of the trade-off is characterized by large magnitudes of trait change leading to functionally divergent specialists and ecological stasis. By contrast, the force extreme of the trade-off is characterized by enhanced ecological lability made possible by phenotypes more readily co-opted for different feeding ecologies. This asymmetry of macroevolutionary outcomes along each extreme is likely the result of an enhanced utility of the pharyngeal jaw system as force-modified oral jaws are adapted for prey that requires intensive processing (e.g., algae, detritus, and mollusks). The velocity-force trade-off, a fundamental feature of many anatomical systems, promotes rapid phenotypic evolution of the surrounding jaw system in a canonical continental adaptive radiation. Considering that the velocity-force trade-off is an inherent feature of all jaw systems that involve a lower element that rotates at a joint, spanning the vast majority of vertebrates, our results may be widely applicable across the tree of life. [Adaptive radiation; constraint; decoupling; jaws; macroevolution; specialization.].

Female cichlids mate with novel androgen receptor mutant males that lack coloration.

A key challenge in animal behavior is disentangling the social stimuli that drive conspecific behaviors. For some species, like teleost fish, putative sexual signaling cues are inextricably linked to others, making it difficult to parse the precise roles distinct signals play in driving conspecific behaviors. In the African cichlid Astatotilapia burtoni, males are either dominant or subordinate, wherein bright coloration, territoriality, and courtship behavior inextricably correlate positively with rank. Here, we leveraged androgen receptor (AR) mutant male A. burtoni that lack dominance-typical coloration but not behavior to isolate the role of male coloration in driving female mating behaviors in this species. We found in independent behavioral assays that females behave aggressively towards AR mutant but not WT males, yet still mated with both types of males. Females showed enhanced activation of esr2b + cells in the hypothalamus when housed with either mutant or WT males and this activation scaled with spawning activities. Therefore, there is not a simple relationship between male coloration and female mating behaviors in A. burtoni, suggesting independent sensory mechanisms converge on hypothalamic esr2b cells to coordinate behavioral output.

Social regulation of arginine vasopressin and oxytocin systems in a wild group-living fish.

The neuropeptides arginine vasopressin (AVP) and oxytocin (OXT) are key regulators of social behaviour across vertebrates. However, much of our understanding of how these neuropeptide systems interact with social behaviour is centred around laboratory studies which fail to capture the social and physiological challenges of living in the wild. To evaluate relationships between these neuropeptide systems and social behaviour in the wild, we studied social groups of the cichlid fish Neolamprologus pulcher in Lake Tanganyika, Africa. We first used SCUBA to observe the behaviour of focal group members and then measured transcript abundance of key components of the AVP and OXT systems across different brain regions. While AVP is often associated with male-typical behaviours, we found that dominant females had higher expression of avp and its receptor (avpr1a2) in the preoptic area of the brain compared to either dominant males or subordinates of either sex. Dominant females also generally had the highest levels of leucyl-cystinyl aminopeptidase (lnpep)-which inactivates AVP and OXT-throughout the brain, potentially indicating greater overall activity (i.e., production, release, and turnover) of the AVP system in dominant females. Expression of OXT and its receptors did not differ across social ranks. However, dominant males that visited the brood chamber more often had lower preoptic expression of OXT receptor a (oxtra) suggesting a negative relationship between OXT signalling and parental care in males of this species. Overall, these results advance our understanding of the relationships between complex social behaviours and neuroendocrine systems under natural settings.

Understanding explosive diversification through cichlid fish genomics.

Owing to their taxonomic, phenotypic, ecological and behavioural diversity and propensity for explosive diversification, the assemblages of cichlid fish in the East African Great Lakes Victoria, Malawi and Tanganyika are important role models in evolutionary biology. With the release of five reference genomes and many additional genomic resources, as well as the establishment of functional genomic tools, the cichlid system has fully entered the genomic era. The in-depth genomic exploration of the East African cichlid fauna - in combination with the examination of their ecology, morphology and behaviour - permits novel insights into the way organisms diversify.