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Evolution: Cichlid Models on the Runaway to Speciation
Abstract
Rapid speciation has fascinated biologists for a long time. A recent study shows that ecological opportunity and sex-biased color differences increase the likelihood of speciation in African cichlid fishes.
... African cichlids constitute the largest extant vertebrate radiation, with several hundreds of species inhabiting lakes and associated river drainages (Turner et al. 2001;Salzburger 2009;Salzburger et al. 2014). Cichlids have thus become favourite model organisms for studying speciation mechanisms and factors that promote or retard diversification (Kocher 2004;Seehausen 2006;Gante & Salzburger 2012;Santos & Salzburger 2012;Wagner et al. 2012). In addition, five species of African cichlids from different lineages and geographical origins have had their genomes recently sequenced (Brawand et al. 2014). ...
... In addition, five species of African cichlids from different lineages and geographical origins have had their genomes recently sequenced (Brawand et al. 2014). One of these lineages, the tribe Lamprologini, comprises almost half of the entire cichlid diversity in Lake Tanganyika (Gante & Salzburger 2012;Wagner et al. 2012). Lamprologines show complex ecological, morphological, trophic and behavioural attributes, representing a radiation within the cichlid radiation (Stiassny 1997). ...
... Lamprologines show complex ecological, morphological, trophic and behavioural attributes, representing a radiation within the cichlid radiation (Stiassny 1997). Unlike other highly diverse cichlid lineages that display extreme levels of sexual dichromatism thought to promote their diversification, such as the radiations of haplochromine cichlids in lakes Malawi and Victoria (Wagner et al. 2012), most lamprologines are sexually monochromatic substrate spawners in which sexes share territorial defence and broodcare (Gante & Salzburger 2012). Furthermore, several examples of introgression have been reported in lamprologine cichlids (e.g. ...
How variation in the genome translates into biological diversity and new species originate has endured as the mystery of mysteries in evolutionary biology. African cichlid fishes are prime model systems to address speciation-related questions for their remarkable taxonomic and phenotypic diversity, and the possible role of gene flow in this process. Here, we capitalize on genome sequencing and phylogenomic analyses to address the relative impacts of incomplete lineage sorting, introgression, and hybrid speciation in the Neolamprologus savoryi-complex (the ‘Princess cichlids’) from Lake Tanganyika. We present a time-calibrated species tree based on whole genome sequences, and provide strong evidence for incomplete lineage sorting in the early phases of diversification and multiple introgression events affecting different stages. Importantly, we find that the Neolamprologus chromosomes show center-to-periphery biases in nucleotide diversity, sequence divergence, GC content, incomplete lineage sorting, and rates of introgression, which are likely modulated by recombination density and linked selection. The detection of heterogeneous genomic landscapes has strong implications on the genomic mechanisms involved in speciation. Collinear chromosomal regions can be protected from gene flow and harbor incompatibility genes if they reside in lowly recombining regions, and coupling can evolve between non-physically linked genomic regions (chromosome centers in particular). Simultaneously, higher recombination toward chromosome peripheries makes these more dynamic, evolvable regions where adaptation polymorphisms have a fertile ground. Hence, differences in genome architecture could explain the levels of taxonomic and phenotypic diversity seen in taxa with collinear genomes, and might have contributed to the spectacular cichlid diversity observed today. This article is protected by copyright. All rights reserved.
... Princess cichlids emerged as prime model systems for studying the evolution of cooperative breeding behavior (Wong and Balshine 2011), and substantial genomic and transcriptomic resources are available (Brawand et al. 2014;Gante et al. 2016). Like most other species of the Tanganyikan cichlid tribe Lamprologini, N. brichardi is sexually monochromatic, that is coloration patterns are identical between males and females (Gante and Salzburger 2012). The dominant, breeding couple is aided by up to 25 subordinate helpers, and the social group is organized in a strict linear hierarchy (Balshine et al. 2001;Zöttl et al. 2013). ...
... Taken together, these findings suggest that social selection may contribute to the dramatic diversity of color patterns (stripes, bars, blotches) observed in many sexually monochromatic cichlids (Gante and Salzburger 2012) as another form of selection shaping diversity in this clade (Salzburger 2009;Muschick et al. 2012). Social selection is expected to drive rapid signal evolution especially in isolated allopatric populations (West-Eberhard 1983;Tanaka 1996). ...
Our understanding of animal communication has been largely driven by advances in theory since empirical evidence has been difficult to obtain. Costly signaling theory became the dominant paradigm explaining the evolution of honest signals, according to which communication reliability relies on differential costs imposed on signalers to distinguish animals of different quality. On the other hand, mathematical models disagree on the source of costs at the communication equilibrium. Here, we present an empirical framework to study the evolution of honest signals that generates predictions on the form, function, and sources of reliability of visual signals. We test these predictions on the facial color patterns of the cooperatively breeding Princess of Burundi cichlid, Neolamprologus brichardi. Using theoretical visual models and behavioral experiments we show that these patterns possess stable chromatic properties for efficient transmission in the aquatic environment, while dynamic changes in signal luminance are used by the fish to communicate switches in aggressive intent. By manipulating signal into out-of-equilibrium expression and simulating a cheater invasion, we demonstrate that social costs (receiver retaliation) promote the honesty of this dynamic conventional signal. By directly probing the sender of a signal in real time, social selection is likely to be the mechanism of choice shaping the evolution of inexpensive, yet reliable context-dependent social signals in general.
... With 1732 valid species (Fricke et al. 2022), Cichlidae are the most species-rich family of freshwater euteleosts (Smith et al. 2008) and a well-known example of exceptional lineage and phenotype diversification among vertebrates (Near et al. 2013;Rabosky et al. 2013). Cichlids are also recognized as excellent models for the investigation of macroevolutionary processes (Gante and Salzburger 2012), particularly adaptive radiation (e.g. Kocher 2004;Young et al. 2009;Wagner et al. 2012;López-Fernández et al. 2013;McGee et al. 2020). ...
Pike cichlids form the largest clade of Neotropical cichlids, with over 100 species presently classified in two genera: Crenicichla (93 species widespread in rivers of South America east of the Andes) and Teleocichla (nine rheophilic Amazonian species). Here, we combined a new dataset of 216 morphological characters with molecular data compiled from published sources, comprising 74 terminal taxa of pike cichlids (68 out of 102 valid species, plus four putative new species), and performed phylogenetic analyses using maximum likelihood, Bayesian inference, and parsimony. Based on a synthesis of our results and previous phylogenies, we propose a new classification in which the clade including all pike cichlids is elevated to the rank of subtribe (Crenicichlina) and the genus Crenicichla is redefined, including three subgenera: Crenicichla (monotypic with the type species), Batrachops (resurected as subgenus), and Lacustria (new subgenus). Teleocichla is maintained as a valid genus and four new genera are proposed: Wallaciia, Saxatilia, Hemeraia, and Lugubria. Our results on character mapping support the hypothesis that resource partitioning in environments with fast-flowing water and rocky beds might have played a role in the origin or maintenance of the great diversity of pike cichlids, resulting in parallel evolution of similar ecomorphs.
... African Great Lakes' cichlids. The most spectacular examples of adaptive radiation in extant vertebrates are arguably the cichlids inhabiting the African Great Lakes (e.g., Gante & Salzburger, 2012). While the cichlid faunas from Lakes Malawi and Victoria are still mostly undescribed and number in the hundreds, the cichlid assemblage from Lake Tanganyika is comparatively well-known. ...
Roughly 18,000 species are described annually as new to science, while estimated extinction rates are comparable to or even exceeding these new discoveries. Considering the estimates of up to 15 million extant eukaryotic species on Earth, of which only about 2 million have been described so far, there has been a recent 'boom' of new potential approaches to more quickly discover and describe the millions of unknown species. This deficit is particularly noted in hyperdiverse taxa, as the current rate of species discovery is considered too slow. Recently, a 'minimalist' alpha taxonomic approach was proposed, relying solely on DNA barcoding and a habitus photograph, in a claimed effort to expedite the naming of new species to combat the so-called taxonomic impediment. In this paper, we point to limitations of minimalist taxonomy, present arguments in favour of the integrative approach, and finally explore a number of potential solutions to combat the taxonomic impediment in hyperdiverse taxa without sacrificing utility and quality for apparent speed and quantity.
... Zokor Divergence and Speciation Momentum. Intrinsic (genetics, demographic history) and extrinsic (climate, habitat) factors could produce speciation momentum (64). Eospalax separated from Myospalax more than 4 Mya, proved by fossil data (8), and Eospalax speciated southwestward to E. baileyi in the QTP about 3.22 Mya (Fig. 5D), when the Kun-Huang tectonism occurred and the QTP had been uplifted (65). ...
Significance
Phylogenies are the basis of many ecological and evolutionary studies. However, zokor phylogeny and speciation patterns are heavily debated. This study disentangled the phylogeny and speciation of zokors genomically. Six species of the Eospalax were separated into high-altitude E. baileyi and E. smithi and the rest four low-altitude species by recent Qinghai-Tibet Plateau uplift 3.6 million y ago. E. rothschildi and E. smithi speciated south of the Qinling–Huaihe Line, where refuges were supplied during glaciation. Introgression and incomplete lineage sorting led to the complex phylogeny of zokors. Genomic islands were formed due to ancient polymorphisms and divergence hitchhiking. This study concluded that climatic, geological, and tectonic events shaped the phylogeny and speciation of zokors in China.
... Intrinsic biological factors also influence whether cichlids radiate, and the colonisation of new lakes and habitats does not automatically result in diversification and radiation (Gante & Salzburger, 2012;Wagner et al., 2012). ...
... A group of fish that has received increasing attention regarding sound production are cichlids. In particular, the cichlid assemblages of the East African Great Lakes are prime models for studying diversification and adaptation due to varied life histories, morphologies and behaviours (Salzburger, 2009;Gante & Salzburger, 2012;Salzburger et al., 2014). While diversity in colour patterns and visual adaptations has long been recognised as a driving force in cichlid evolution (Santos & Salzburger, 2012;Wagner et al., 2012), the description of sound production and hearing abilities have only more recently gained momentum in spite of a long history of research (Amorim, 2006;Ladich & Fay, 2013). ...
Teleost fishes not only communicate with well-known visual cues, but also olfactory and acoustic signals. Communicating with sound has advantages, as acoustic signals propagate fast, omnidirectionally, around obstacles and over long distances. Heterogeneous environments might favour multimodal communication, especially in socially complex species, as the combination of modalities’ strengths helps overcome their individual limitations. Fishes of the ecologically and morphologically diverse family Cichlidae are known to be vocal. Here we investigated sound production in the socially complex Princess cichlid Neolamprologus pulcher from Lake Tanganyika in East Africa. We show that wild and captive N. pulcher produce only short-duration, broadband high-frequency sounds (mean: 12 kHz), when stimulated by mirror images. The evolutionary reasons for this “low frequency silencing” are still unclear. In laboratory experiments, N. pulcher produced distinct two-pulsed calls mostly, but not exclusively, associated with agonistic displays. Princess cichlids produce these high-frequency sounds both in combination with and independent from visual displays, suggesting that sounds are not a by-product of behavioural displays. Further studies on the hearing abilities of N. pulcher are needed to clarify whether the high-frequency sounds are used in intra- or inter-specific communication.
... Our analyses did not detect any form of population or kin structuring, suggesting that nine-spined sticklebacks from the different habitats in the study lake were all members of a single panmictic population. While this may not be surprising given the small size and relatively young age of this postglacial lake, it is worth noting that sympatric speciation, or at least a strong within-lake population structuring, is fairly common in fish (Kocher 2004;Stauffer and van Snick Gray 2004;Gante and Salzburger 2012;Ford et al. 2015;Seehausen 2015), even in postglacial habitats (Schluter 1996b;Hendry et al. 2013;McGee et al. 2013). This type of population structuring is typically associated with trophic niche differentiation between the divergent forms, for example, in the threespined stickleback (Gasterosteus aculeatus; Schluter 1993), a close relative of the nine-spined stickleback. ...
Specialization for the use of different resources can lead to ecological speciation. Accordingly, there are numerous examples of ecologically specialized pairs of fish “species” in postglacial lakes. Using a polymorphic panel of single nucleotide variants, we tested for genetic footprints of within-lake population stratification in nine-spined sticklebacks (Pungitius pungitius) collected from three habitats (viz. littoral, benthic, and pelagic) within a northern Swedish lake. Analyses of admixture, population structure, and relatedness all supported the conclusion that the fish from this lake form a single interbreeding unit. © 2016 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
... In Lake Tanganyika, five tribes of the family Cichlidae (Tropheini, Lamprologini, Ectodini, Eretmodini, and Tilapini) have acquired several ecomorphs that are closely related to feeding habits in herbivory such as grazing, browsing, scraping, biting, and scooping [10][11][12][13]. These tribes have no sexual dichromatism, and therefore, we can focus on the effect of ecological opportunity in the adaptive radiation of these herbivorous cichlids [14,15]. Grazers, browsers, and scrapers are highly specialised and diversified, especially in these herbivorous habits [16]. ...
Background
Lake Tanganyika, an ancient lake in the Great Rift Valley, is famous for the adaptive radiation of cichlids. Five tribes of the Cichlidae family have acquired herbivory, with five ecomorphs: grazers, browsers, scrapers, biters, and scoopers. Sixteen species of the herbivorous cichlids coexist on a rocky littoral slope in the lake. Seven of them individually defend feeding territories against intruding herbivores to establish algal farms. We collected epiphyton from these territories at various depths and also gathered fish specimens. Algal and cyanobacteria community structures were analysed using the amplicon-metagenomic method.ResultsBased on 454-pyrosequencing of SSU rRNA gene sequences, we identified 300 phototrophic taxa, including 197 cyanobacteria, 57 bacillariophytes, and 31 chlorophytes. Algal farms differed significantly in their composition among cichlid species, even in the same ecomorph, due in part to their habitat-depth segregation. The algal species composition of the stomach contents and algal farms of each species differed, suggesting that cichlids selectively harvest their farms. The stomach contents were highly diverse, even between species in the same tribe, in the same feeding ecomorph.Conclusions
In this study, the amplicon-metagenomic approach revealed food niche separation based on habitat-depth segregation among coexisting herbivorous cichlids in the same ecomorphs in Lake Tanganyika.
... While there is no doubt that colour-mediated mate choice contributes to cichlid speciation, other factors (such as ecological opportunity and geographic structure) are important as well, and may interact with sexual selection. The relative importance of these mechanisms may vary over evolutionary time and differ between lineages [132,154]. ...
Cichlid fishes constitute one of the most species-rich families of vertebrates. In addition to complex social behaviour and morphological versatility, they are characterised by extensive diversity in coloration, both within and between species. Here, we review the cellular and molecular mechanisms underlying colour variation in this group and the selective pressures responsible for the observed variation. We specifically address the evidence for the hypothesis that divergence in coloration is associated with the evolution of reproductive isolation between lineages. While we conclude that cichlid colours are excellent models for understanding the role of animal communication in species divergence, we also identify taxonomic and methodological biases in the current research effort. We suggest that the integration of genomic approaches with ecological and behavioural studies, across the entire cichlid family and beyond it, will contribute to the utility of the cichlid model system for understanding the evolution of biological diversity.
Based on morphological and molecular analyses of a Petrochromis fish (Cichlidae) from the southern end of Lake Tanganyika, this fish is considered a taxonomic species distict from six known congeners. A new scientific name is proposed for this fish. A key to the seven Petrochromis species is included.
The infraorbitals (IOs) of four species endemic to Lake Tanganyika were examined and on the basis of this information and previous morphological and molecular studies, the tribe Greenwoodochromini is synonymized with the tribe Limnochromini and a new combination for Limnochromis abeelei and Limnochromis staneri is proposed: Greenwoodochromis abeelei and Greenwoodochromis staneri. The revised tribe Limnochromini, comprising 10 species belonging to seven genera, is characterized by IOs representing types G and I. The revised genus Greenwoodochromis, which consists of four species, is characterized by IOs representing type I.
In order to understand the nervous system, it is necessary to know the synaptic connections between the neurons, yet to date,
only the wiring diagram of the adult hermaphrodite of the nematode Caenorhabditis elegans has been determined. Here, we present the wiring diagram of the posterior nervous system of the C. elegans adult male, reconstructed from serial electron micrograph sections. This region of the male nervous system contains the sexually
dimorphic circuits for mating. The synaptic connections, both chemical and gap junctional, form a neural network with four
striking features: multiple, parallel, short synaptic pathways directly connecting sensory neurons to end organs; recurrent
and reciprocal connectivity among sensory neurons; modular substructure; and interneurons acting in feedforward loops. These
features help to explain how the network robustly and rapidly selects and executes the steps of a behavioral program on the
basis of the inputs from multiple sensory neurons.
A fundamental challenge to our understanding of biodiversity is to explain why some groups of species undergo adaptive radiations, diversifying extensively into many and varied species, whereas others do not. Both extrinsic environmental factors (for example, resource availability, climate) and intrinsic lineage-specific traits (for example, behavioural or morphological traits, genetic architecture) influence diversification, but few studies have addressed how such factors interact. Radiations of cichlid fishes in the African Great Lakes provide some of the most dramatic cases of species diversification. However, most cichlid lineages in African lakes have not undergone adaptive radiations. Here we compile data on cichlid colonization and diversification in 46 African lakes, along with lake environmental features and information about the traits of colonizing cichlid lineages, to investigate why adaptive radiation does and does not occur. We find that extrinsic environmental factors related to ecological opportunity and intrinsic lineage-specific traits related to sexual selection both strongly influence whether cichlids radiate. Cichlids are more likely to radiate in deep lakes, in regions with more incident solar radiation and in lakes where there has been more time for diversification. Weak or negative associations between diversification and lake surface area indicate that cichlid speciation is not constrained by area, in contrast to diversification in many terrestrial taxa. Among the suite of intrinsic traits that we investigate, sexual dichromatism, a surrogate for the intensity of sexual selection, is consistently positively associated with diversification. Thus, for cichlids, it is the coincidence between ecological opportunity and sexual selection that best predicts whether adaptive radiation will occur. These findings suggest that adaptive radiation is predictable, but only when species traits and environmental factors are jointly considered.
Mechanisms of speciation in cichlid fish were investigated by analyzing population genetic models of sexual selection on sex-determining
genes associated with color polymorphisms. The models are based on a combination of laboratory experiments and field observations
on the ecology, male and female mating behavior, and inheritance of sex-determination and color polymorphisms. The models
explain why sex-reversal genes that change males into females tend to be X-linked and associated with novel colors, using the hypothesis of restricted recombination on the sex chromosomes, as suggested
by previous theory on the evolution of recombination. The models reveal multiple pathways for rapid sympatric speciation through
the origin of novel color morphs with strong assortative mating that incorporate both sex-reversal and suppressor genes. Despite
the lack of geographic isolation or ecological differentiation, the new species coexists with the ancestral species either
temporarily or indefinitely. These results may help to explain different patterns and rates of speciation among groups of
cichlids, in particular the explosive diversification of rock-dwelling haplochromine cichlids.
Key wordscichlid fish–restricted recombination–sex chromosomes–sex ratio–sex reversal–sexual selection–sympatric speciation
Mechanisms of speciation in cichlid fish were investigated by analyzing population genetic models of sexual selection on sex-determining genes associated with color polymorphisms. The models are based on a combination of laboratory experiments and field observations on the ecology, male and female mating behavior, and inheritance of sex-determination and color polymorphisms. The models explain why sex-reversal genes that change males into females tend to be X-linked and associated with novel colors, using the hypothesis of restricted recombination on the sex chromosomes, as suggested by previous theory on the evolution of recombination. The models reveal multiple pathways for rapid sympatric speciation through the origin of novel color morphs with strong assortative mating that incorporate both sex-reversal and suppressor genes. Despite the lack of geographic isolation or ecological differentiation, the new species coexists with the ancestral species either temporarily or indefinitely. These results may help to explain different patterns and rates of speciation among groups of cichlids, in particular the explosive diversification of rock-dwelling haplochromine cichlids.
Empirical data indicate that sexual preferences are critical for maintaining species boundaries, yet theoretical work has suggested that, on their own, they can have only a minimal role in maintaining biodiversity. This is because long-term coexistence within overlapping ranges is thought to be unlikely in the absence of ecological differentiation. Here we challenge this widely held view by generalizing a standard model of sexual selection to include two ubiquitous features of populations with sexual selection: spatial variation in local carrying capacity, and mate-search costs in females. We show that, when these two features are combined, sexual preferences can single-handedly maintain coexistence, even when spatial variation in local carrying capacity is so slight that it might go unnoticed empirically. This theoretical study demonstrates that sexual selection alone can promote the long-term coexistence of ecologically equivalent species with overlapping ranges, and it thus provides a novel explanation for the maintenance of species diversity.
The hundreds of endemic species of cichlid fishes in the East African Great Lakes Tanganyika, Malawi, and Victoria are a prime model system in evolutionary biology. With five genomes currently being sequenced, eastern African cichlids also represent a forthcoming genomic model for evolutionary studies of genotype-to-phenotype processes in adaptive radiations. Here we report the functional annotation and comparative analyses of transcriptome data sets for two eastern African cichlid species, Astatotilapia burtoni and Ophthalmotilapia ventralis, representatives of the modern haplochromines and ectodines, respectively. Nearly 647,000 expressed sequence tags were assembled in more than 46,000 contigs for each species using the 454 sequencing technology, largely expanding the current sequence data set publicly available for these cichlids. Total predicted coverage of their proteome diversity is approximately 50% for both species. Comparative qualitative and quantitative analyses show very similar transcriptome data for the two species in terms of both functional annotation and relative abundance of gene ontology terms expressed. Average genetic distance between species is 1.75% when all transcript types are considered including nonannotated sequences, 1.33% for annotated sequences only including untranslated regions, and decreases to nearly half, 0.95%, for coding sequences only, suggesting a large contribution of noncoding regions to their genetic diversity. Comparative analyses across the two species, tilapia and the outgroup medaka based on an overlapping data set of 1,216 genes (∼526 kb) demonstrate cichlid-specific signature of disruptive selection and provide a set of candidate genes that are putatively under positive selection. Overall, these data sets offer the genetic platform for future comparative analyses in light of the upcoming genomes for this taxonomic group.
Sexual Blotch
Sexual conflicts may provide selection pressures that facilitate invasion of new genetic sex determiners. Roberts et al. (p. 998 , published online 1 October) describe data obtained from several species of sexually dimorphic cichlid fishes found in Lake Malawi that support this model. An orangeblotch color pattern has evolved among the females of rock-dwelling species because it provides effective camouflage against the algae-coated rocks. Blotched males (OB) are rare, possibly because the trait interferes with the normal male color pattern of blue stripes that are important cues for mate selection. The pigmentation pattern that creates this conflict between natural selection in females and sexual selection in males is caused by mutation in the cis -regulatory region of the Pax7 gene and is tightly linked to a dominant female sex determiner. When bred in the lab, the OB males inherit the intact maternal OB haplotype and their OB-carrying chromosome determines female sex in the offspring; the males seem to be sex-reversed by another mechanism.
Theoretically, divergent selection on sensory systems can cause speciation through sensory drive. However, empirical evidence is rare and incomplete. Here we demonstrate sensory drive speciation within island populations of cichlid fish. We identify the ecological and molecular basis of divergent evolution in the cichlid visual system, demonstrate associated divergence in male colouration and female preferences, and show subsequent differentiation at neutral loci, indicating reproductive isolation. Evidence is replicated in several pairs of sympatric populations and species. Variation in the slope of the environmental gradients explains variation in the progress towards speciation: speciation occurs on all but the steepest gradients. This is the most complete demonstration so far of speciation through sensory drive without geographical isolation. Our results also provide a mechanistic explanation for the collapse of cichlid fish species diversity during the anthropogenic eutrophication of Lake Victoria.
Lake Tanganyika, the oldest of the East African Great Lakes, harbors the ecologically, morphologically, and behaviorally most complex of all assemblages of cichlid fishes, consisting of about 200 described species. The evolutionary old age of the cichlid assemblage, its extreme degree of morphological differentiation, the lack of species with intermediate morphologies, and the rapidity of lineage formation have made evolutionary reconstruction difficult. The number and origin of seeding lineages, particularly the possible contribution of riverine haplochromine cichlids to endemic lacustrine lineages, remains unclear. Our phylogenetic analyses, based on mitochondrial DNA sequences of three gene segments of 49 species (25% of all described species, up to 2,400 bp each), yield robust phylogenies that provide new insights into the Lake Tanganyika adaptive radiation as well as into the origin of the Central- and East-African haplochromine faunas. Our data suggest that eight ancient African lineages may have seeded the Tanganyikan cichlid radiation. One of these seeding lineages, probably comprising substrate spawning Lamprologus-like species, diversified into six lineages that evolved mouthbrooding during the initial stage of the radiation. All analyzed haplochromines from surrounding rivers and lakes seem to have evolved within the radiating Tanganyikan lineages. Thus, our findings contradict the current hypothesis that ancestral riverine haplochromines colonized Lake Tanganyika to give rise to at least part of its spectacular endemic cichlid species assemblage. Instead, the early phases of the Tanganyikan radiation affected Central and East African rivers and lakes. The haplochromines may have evolved in the Tanganyikan basin before the lake became a hydrologically and ecologically closed system and then secondarily colonized surrounding rivers. Apparently, therefore, the current diversity of Central and East African haplochromines represents a relatively young and polyphyletic fauna that evolved from or in parallel to lineages now endemic to Lake Tanganyika.
Adaptive radiation is defined as the evolution of ecological and phenotypic diversity within a rapidly multiplying lineage. When it occurs, adaptive radiation typically follows the colonization of a new environment or the establishment of a “key innovation,” which opens new ecological niches and/or new paths for evolution. Here, we take advantage of recent developments in speciation theory and modern computing power to build and explore a large-scale, stochastic, spatially explicit, individual-based model of adaptive radiation driven by adaptation to multidimensional ecological niches. We are able to model evolutionary dynamics of populations with hundreds of thousands of sexual diploid individuals over a time span of 100,000 generations assuming realistic mutation rates and allowing for genetic variation in a large number of both selected and neutral loci. Our results provide theoretical support and explanation for a number of empirical patterns including “area effect,” “overshooting effect,” and “least action effect,” as well as for the idea of a “porous genome.” Our findings suggest that the genetic architecture of traits involved in the most spectacular radiations might be rather simple. We show that a great majority of speciation events are concentrated early in the phylogeny. Our results emphasize the importance of ecological opportunity and genetic constraints in controlling the dynamics of adaptive radiation.
• ecological
• modeling
• speciation
• diversification
• parapatric
Whether interspecific hybridization is important as a mechanism that generates biological diversity is a matter of controversy. Whereas some authors focus on the potential of hybridization as a source of genetic variation, functional novelty and new species, others argue against any important role, because reduced fitness would typically render hybrids an evolutionary dead end. By drawing on recent developments in the genetics and ecology of hybridization and on principles of ecological speciation theory, I develop a concept that reconciles these views and adds a new twist to this debate. Because hybridization is common when populations invade new environments and potentially elevates rates of response to selection, it predisposes colonizing populations to rapid adaptive diversification under disruptive or divergent selection. I discuss predictions and suggest tests of this hybrid swarm theory of adaptive radiation and review published molecular phylogenies of adaptive radiations in light of the theory.
Incipient speciation in a population occupying a continuous range is modeled as the joint evolution of geographic variation in female mating preferences and a quantitative secondary sexual character of males. Genetic variance in both traits is assumed to be maintained within local populations by polygenic mutation and recombination. Three types of polygamous mating systems are analyzed. Sexual isolation and character divergence can originate rapidly over a wide geographic range, driven by genetic instability of the mating system in local populations. During this process, clines forming around a sharp ecological boundary are always monotonic. Even in the absence of genetic instability, the evolution of female mating preferences can greatly amplify large-scale geographic variation in male secondary sexual characters and produce widespread sexual isolation with no geographic discontinuity. These conclusions contrast with the popular conception that premating isolation is selected initially only in the contact zone between races to avoid deleterious hybridization, later spreading slowly if at all to other regions.-from Author
Incipient speciation in a population occupying a continuous range is modeled as the joint evolution of geographic variation in female mating preferences and a quantitative secondary sexual character of males. Genetic variance in both traits is assumed to be maintained within local populations by polygenic mutation and recombination. Three types of polygamous mating systems are analyzed. The models show that sexual isolation and character divergence can originate rapidly over a wide geographic range, driven by genetic instability of the mating system in local populations. During this process, clines forming around a sharp ecological boundary are always monotonic. Even in the absence of genetic instability, the evolution of female mating preferences can greatly amplify large-scale geographic variation in male secondary sexual characters and produce widespread sexual isolation with no geographic discontinuity. These conclusions contrast with the popular conception that premating isolation is selected initially only in the contact zone between races to avoid deleterious hybridization, later spreading slowly if at all to other regions.
The evolution of sexual dimorphism in quantitative characters under natural and sexual selection acting differently on the sexes is analyzed using population genetics models. The effects of genes when in males may be correlated with their effects when in females, producing correlated selective responses between the sexes, so that male and female phenotypes cannot evolve independently But under weak natural selection with constant relative fitnesses, in the absence of sexual selection, the joint evolution of the mean phenotypes of the sexes increases the mean fitness in a population, and if there is genetic variation for sexual dimorphism each sex eventually achieves a locally optimum phenotype. With sexual selection, fitnesses are generally frequency-dependent and evolution of the mean phenotypes does not maximize the mean fitness. Provided individual fitnesses exist, at equilibrium natural and sexual selection balance in each sex. A moderate intensity of sexual selection acting on a character under weak natural selection toward an intermediate optimum phenotype can produce a large deviation of the mean phenotype from the optimum and a substantial decrease of the mean fitness in a population, increasing the probability of extinction. When homologous characters in males and females vary similarly and are highly correlated genetically, the rate of evolution of sexual dimorphism may be one or more orders of magnitude slower than that for the average phenotype in a population. Methods for partitioning sexual dimorphism into contributions from natural and sexual selection are discussed, and genetic experiments are suggested for testing the involvement of non-equilibrium correlated selective responses between the sexes in observed cases of sexual dimorphism.
The joint evolution of female mating preferences and secondary sexual characters of males is modeled for polygamous species in which males provide only genetic material to the next generation and females have many potential mates to choose among. Despite stabilizing natural selection on males, various types of mating preferences may create a runaway process in which the outcome of phenotypic evolution depends critically on the genetic variation parameters and initial conditions of a population. Even in the absence of genetic instability, rapid evolution can result from an interaction of natural and sexual selection with random genetic drift along lines of equilibria. The models elucidate genetic mechanisms that can initiate or contribute to rapid speciation by sexual isolation and divergence of secondary sexual characters.
Rapid speciation can occur on ecological time scales and interfere with ecological processes, resulting in species distribution patterns that are difficult to reconcile with ecological theory. The haplochromine cichlids in East African lakes are an extreme example of rapid speciation. We analyse the causes of their high speciation rates. Various studies have identified disruptive sexual selection acting on colour polymorphisms that might cause sympatric speciation. Using data on geographical distribution, colouration and relatedness from 41 species endemic to Lake Victoria, we test predictions from this hypothesis. Plotting numbers of pairs of closely related species against the amount of distributional overlap between the species reveals a bimodal distribution with modes on allopatric and sympatric. The proportion of sister species pairs that are heteromorphic for the traits under disruptive selection is higher in sympatry than in allopatry. These data support the hypothesis that disruptive sexual selection on colour polymorphisms has caused sympatric speciation and help to explain the rapid radiation of haplochromine species flocks.
Through adaptive radiation, ancestral species rapidly diversify into multiple species with different ecological adaptations. The haplochromine cichlid fishes of the East African Great Lakes are considered classic examples of adaptive radiation, but our understanding of the evolutionary origins of these radiations has been limited by inadequate taxonomic and genomic sampling 1 and 2. Perhaps the largest of these radiations is from Lake Malawi, estimated to contain between 500 and 800 endemic species. Surprisingly, its monophyly — the origin from a single ancestral species — has never been critically tested. This is because river populations which could have seeded the radiation, with one very limited exception [3], have never been included in phylogenetic reconstructions. Moreover, phylogenies have relied heavily on mitochondrial DNA (mtDNA), which can be a misleading phylogenetic marker for species capable of hybridization 4 and 5 because its non-recombining nature means that transfer to other species can occur via asymmetric introgression and ‘allele surfing’ [6]. Here, we used broad taxonomic sampling and nuclear DNA markers with wide genomic coverage and find that the Lake Malawi radiation is not monophyletic, but instead contains genetic material from divergent riverine ancestors indicating multiple invasions and hybridization.
The question of how genetic variation translates into organismal diversity has puzzled biologists for decades. Despite recent advances in evolutionary and developmental genetics, the mechanisms that underlie adaptation, diversification and evolutionary innovation remain largely unknown. The exceptionally diverse species flocks of cichlid fishes are textbook examples of adaptive radiation and explosive speciation and emerge as powerful model systems to study the genetic basis of animal diversification. East Africa's hundreds of endemic cichlid species are akin to a natural mutagenesis screen and differ greatly not only in ecologically relevant (hence naturally selected) characters such as mouth morphology and body shape, but also in sexually selected traits such as coloration. One of the most fascinating aspects of cichlid evolution is the frequent occurrence of evolutionary parallelisms, which has led to the question whether selection alone is sufficient to produce these parallel morphologies, or whether a developmental or genetic bias has influenced the direction of diversification. Here, I review fitness-relevant traits that could be responsible for the cichlids' evolutionary success and assess whether these were shaped by sexual or natural selection. I then focus on the interaction and the relative importance of sexual vs. natural selection in cichlid evolution. Finally, I discuss what is currently known about the genes underlying the morphogenesis of adaptively relevant traits and highlight the importance of the forthcoming cichlid genomes in the quest of the genetic basis of diversification in this group.
Studying the neural basis of decision-making has largely taken one of two paths: one has involved cell-by-cell characterization of neuronal circuits in invertebrates; and the other, single-unit studies of monkeys performing cognitive tasks. Here I shall attempt to bring these two disparate approaches together.
The joint evolution of female mating preferences and secondary sexual characters of males is modeled for polygamous species in which males provide only genetic material to the next generation and females have many potential mates to choose among. Despite stabilizing natural selection on males, various types of mating preferences may create a runaway process in which the outcome of phenotypic evolution depends critically on the genetic variation parameters and initial conditions of a population. Even in the absence of genetic instability, rapid evolution can result from an interaction of natural and sexual selection with random genetic drift along lines of equilibria. The models elucidate genetic mechanisms that can initiate or contribute to rapid speciation by sexual isolation and divergence of secondary sexual characters.
Cichlids and All Other Fishes of Lake Tanganyika
- P. Brichard
- P. Brichard
Sexual selection enables
- M Gonigle
- L K Mazzucco
- R Otto
- S P Dieckmann
M'Gonigle, L.K., Mazzucco, R., Otto, S.P., and Dieckmann, U. (2012). Sexual selection enables
Dynamic patterns of adaptive radiation
- Gavrilets
Gavrilets, S., and Vose, A. (2005). Dynamic
patterns of adaptive radiation. Proc. Natl. Acad.
Hybridization and adaptive radiation
- Seehausen
Repeated colonization and hybridization in Lake Malawi cichlids
- Joyce