Rapid Adaptive Radiation Research Articles

Ciliary Rootlet Coiled-Coil 2 (crocc2) Is Associated with Evolutionary Divergence and Plasticity of Cichlid Jaw Shape.

Cichlid fishes exhibit rapid, extensive, and replicative adaptive radiation in feeding morphology. Plasticity of the cichlid jaw has also been well documented, and this combination of iterative evolution and developmental plasticity has led to the proposition that the cichlid feeding apparatus represents a morphological “flexible stem.” Under this scenario, the fixation of environmentally sensitive genetic variation drives evolutionary divergence along a phenotypic axis established by the initial plastic response. Thus, if plasticity is predictable then so too should be the evolutionary response. We set out to explore these ideas at the molecular level by identifying genes that underlie both the evolution and plasticity of the cichlid jaw. As a first step, we fine-mapped an environment-specific quantitative trait loci for lower jaw shape in cichlids, and identified a nonsynonymous mutation in the ciliary rootlet coiled-coil 2 (crocc2), which encodes a major structural component of the primary cilium. Given that primary cilia play key roles in skeletal mechanosensing, we reasoned that this gene may confer its effects by regulating the sensitivity of bone to respond to mechanical input. Using both cichlids and zebrafish, we confirmed this prediction through a series of experiments targeting multiple levels of biological organization. Taken together, our results implicate crocc2 as a novel mediator of bone formation, plasticity, and evolution.

Identification of a novel sex determining chromosome in cichlid fishes that acts as XY or ZW in different lineages

Sex determination systems are highly conserved among most vertebrates with genetic sex determination, but can be variable and evolve rapidly in some. Here, we study sex determination in a clade with exceptionally high sex chromosome turnover rates. We identify the sex determining chromosomes in three interspecific crosses of haplochromine cichlid fishes from Lakes Victoria and Malawi. We find evidence for different sex determiners in each cross. In the Malawi cross and one Victoria cross the same chromosome is sex-linked but while females are the heterogametic sex in the Malawi species, males are the heterogametic sex in the Victoria species. This chromosome has not previously been reported to be sex determining in cichlids, increasing the number of different chromosomes shown to be sex determining in cichlids to 12. All Lake Victoria species of our crosses are less than 15,000 years divergent, and we identified different sex determiners among them. Our study provides further evidence for the diversity and evolutionary flexibility of sex determination in cichlids, factors which might contribute to their rapid adaptive radiations.

Senecio as a model system for integrating studies of genotype, phenotype and fitness.

Two major developments have made it possible to use examples of ecological radiations as model systems to understand evolution and ecology. First, the integration of quantitative genetics with ecological experiments allows detailed connections to be made between genotype, phenotype, and fitness in the field. Second, dramatic advances in molecular genetics have created new possibilities for integrating field and laboratory experiments with detailed genetic sequencing. Combining these approaches allows evolutionary biologists to better study the interplay between genotype, phenotype, and fitness to explore a wide range of evolutionary processes. Here, we present the genus Senecio (Asteraceae) as an excellent system to integrate these developments, and to address fundamental questions in ecology and evolution. Senecio is one of the largest and most phenotypically diverse genera of flowering plants, containing species ranging from woody perennials to herbaceous annuals. These Senecio species exhibit many growth habits, life histories, and morphologies, and they occupy a multitude of environments. Common within the genus are species that have hybridized naturally, undergone polyploidization, and colonized diverse environments, often through rapid phenotypic divergence and adaptive radiation. These diverse experimental attributes make Senecio an attractive model system in which to address a broad range of questions in evolution and ecology.

Homology conundrum among foreguts of caenogastropod molluscs: A view from comparative patterns of development

AbstractEvolution of two novel feeding strategies among caenogastropod molluscs, suspension feeding in calyptraeids such as Crepidula fornicata and predatory feeding with a pleurembolic proboscis among neogastropods, may have both involved elongation of the anterior esophagus. Emergence of predatory feeding with a proboscis is particularly significant because it correlates with the rapid adaptive radiation of buccinoidean and muricoidean neogastropods during the Cretaceous. However, the notion that this important evolutionary transition involved elongation of the anterior esophagus to extend down a long proboscis has been disputed by evidence that it may have been the wall of the buccal cavity that elongated. We undertook a comparative study on foregut morphogenesis during larval and metamorphic development in C. fornicata and in three species of neogastropods with a pleurembolic proboscis to examine the hypothesis that the same region of foregut has elongated in all. We approached this by identifying a conserved marker for the boundary between buccal cavity and anterior esophagus, which was recognizable before the developing foregut showed regional differences in length. A survey of four species of littorinimorph caenogastropods suggested that the site of neurogenic placodes for the buccal ganglia could serve as this marker. Results showed that foregut lengthening in C. fornicata involved elongation posterior to neurogenic placodes for buccal ganglia, an area that corresponded to the anterior esophagus in the other littorinimorphs. However, foregut elongation occurred anterior to neurogenic placodes for buccal ganglia in two buccinoidean and one muricoidean neogastropod. The elongated foregut within the pleurembolic proboscis of these neogastropods qualifies as anterior esophagus only if the definition of the anterior esophagus is expanded to include the dorsal folds that run down the roof of the buccal cavity. Regardless of how the anterior esophagus is defined, comparative developmental data do not support the hypothesis of homology between the elongated adult foregut regions in C. fornicata and in neogastropods with a pleurembolic proboscis.

High diversity of fish ectoparasitic monogeneans (Dactylogyrus) in the Iberian Peninsula: a case of adaptive radiation?

The epicontinental fauna of the Iberian Peninsula is strongly influenced by its geographical history. As the possibilities for dispersion of organisms into and from this region were (and still are) limited, the local fauna consists almost exclusively of endemic species. Almost all Iberian freshwater fishes of the families Leuciscidae and Cyprinidae are endemic and on-going research on these taxa continually uncovers new species. Nevertheless, information on their host-specific parasites remains scarce. In this study, we investigate the diversity and phylogenetic relationships in monogeneans of the genus Dactylogyrus (gill ectoparasites specific to cyprinoid fish) in the Iberian Peninsula. Twenty-two species were collected and identified from 19 host species belonging to Cyprinidae and Leuciscidae. A high degree of endemism was observed, with 21 Dactylogyrus species reported from Iberia only and a single species, D. borealis, also reported from other European regions. Phylogenetic analysis split the endemic Iberian Dactylogyrus into two well-supported clades, the first encompassing Dactylogyrus parasitizing endemic Luciobarbus spp. only, and the second including all Dactylogyrus species of endemic leuciscids and four species of endemic cyprinids. Species delimitation analysis suggests a remarkable diversity and existence of a multitude of cryptic Dactylogyrus species parasitizing endemic leuciscids (Squalius spp. and representatives of Chondrostoma s.l.). These results suggest a rapid adaptive radiation of Dactylogyrus in this geographically isolated region, closely associated with their cyprinoid hosts. Moreover, phylogenetic analysis supports that Dactylogyrus parasites colonized the Iberian Peninsula through multiple dispersion events.

Differential Expression in Testis and Liver Transcriptomes from Four Species of Peromyscus (Rodentia: Cricetidae).

The genus Peromyscus represents a rapidly diverged clade of Cricetid rodents that contains multiple cryptic species and has a propensity for morphologic conservation across its members. The unresolved relationships in previously proposed phylogenies reflect a suspected rapid adaptive radiation. To identify functional groups of genes that may be important in reproductive isolation in a reoccurring fashion across the Peromyscus phylogeny, liver and testis transcriptomes from four species (P. attwateri, P. boylii, P. leucopus, and P. maniculatus) were generated and differential expression (DE) tests were conducted. Taxa were selected to represent members diverged from a common ancestor: P. attwateri + P. boylii (clade A), and P. leucopus + P. maniculatus (clade B). Comparison of clades (A vs. B) suggested that 252 transcripts had significant DE in the liver data set, whereas significant DE was identified for 657 transcripts in the testis data set. Further, 45 genes had DE isoforms in the 657 testis transcripts and most of these functioned in major reproductive roles such as acrosome assembly, spermatogenesis, and cell cycle processes (meiosis). DE transcripts in the liver mapped to more broad gene ontology terms (metabolic processes, catabolic processes, response to chemical, and regulatory processes), and DE transcripts in the testis mapped to gene ontology terms associated with reproductive processes, such as meiosis, sperm motility, acrosome assembly, and sperm–egg fusion. These results suggest that a suite of genes that conduct similar functions in the testes may be responsible for the adaptive radiation events and potential reoccurring speciation of Peromyscus in terms of reproduction through varying expression levels.

The coincidence of ecological opportunity with hybridization explains rapid adaptive radiation in Lake Mweru cichlid\xa0fishes

The process of adaptive radiation was classically hypothesized to require isolation of a lineage from its source (no gene flow) and from related species (no competition). Alternatively, hybridization between species may generate genetic variation that facilitates adaptive radiation. Here we study haplochromine cichlid assemblages in two African Great Lakes to test these hypotheses. Greater biotic isolation (fewer lineages) predicts fewer constraints by competition and hence more ecological opportunity in Lake Bangweulu, whereas opportunity for hybridization predicts increased genetic potential in Lake Mweru. In Lake Bangweulu, we find no evidence for hybridization but also no adaptive radiation. We show that the Bangweulu lineages also colonized Lake Mweru, where they hybridized with Congolese lineages and then underwent multiple adaptive radiations that are strikingly complementary in ecology and morphology. Our data suggest that the presence of several related lineages does not necessarily prevent adaptive radiation, although it constrains the trajectories of morphological diversification. It might instead facilitate adaptive radiation when hybridization generates genetic variation, without which radiation may start much later, progress more slowly or never occur.

The paradox behind the pattern of rapid adaptive radiation: how can the speciation process sustain itself through an early burst?

Rapid adaptive radiation poses a distinct question apart from speciation and adaptation: what happens after one speciation event? That is, how are some lineages able to continue speciating through a rapid burst? This question connects global macroevolutionary patterns to microevolutionary processes. Here we review major features of rapid radiations in nature and their mismatch with theoretical models and what is currently known about speciation mechanisms. Rapid radiations occur on three major diversification axes - species richness, phenotypic disparity, and ecological diversity - with exceptional outliers on each axis. The paradox is that the hallmark early stage of adaptive radiation, a rapid burst of speciation and niche diversification, is contradicted by most existing speciation models which instead predict continuously decelerating speciation rates and niche subdivision through time. Furthermore, while speciation mechanisms such as magic traits, phenotype matching, and physical linkage of co-adapted alleles promote speciation, it is often not discussed how these mechanisms could promote multiple speciation events in rapid succession. Additional mechanisms beyond ecological opportunity are needed to understand how rapid radiations occur. We review the evidence for five emerging theories: 1) the 'transporter' hypothesis: introgression and the ancient origins of adaptive alleles, 2) the 'signal complexity' hypothesis: the dimensionality of sexual traits, 3) the connectivity of fitness landscapes, 4) 'diversity begets diversity', and 5) flexible stem/'plasticity first'. We propose new questions and predictions to guide future work on the mechanisms underlying the rare origins of rapid radiation.

Adaptive Radiation from a Chromosomal Perspective: Evidence of Chromosome Set Stability in Cichlid Fishes (Cichlidae: Teleostei) from the Barombi Mbo Lake, Cameroon.

Cichlid fishes are the subject of scientific interest because of their rapid adaptive radiation, resulting in extensive ecological and taxonomic diversity. In this study, we examined 11 morphologically distinct cichlid species endemic to Barombi Mbo, the largest crater lake in western Cameroon, namely Konia eisentrauti, Konia dikume, Myaka myaka, Pungu maclareni, Sarotherodon steinbachi, Sarotherodon lohbergeri, Sarotherodon linnellii, Sarotherodon caroli, Stomatepia mariae, Stomatepia pindu, and Stomatepia mongo. These species supposedly evolved via sympatric ecological speciation from a common ancestor, which colonized the lake no earlier than one million years ago. Here we present the first comparative cytogenetic analysis of cichlid species from Barombi Mbo Lake using both conventional (Giemsa staining, C-banding, and CMA3/DAPI staining) and molecular (fluorescence in situ hybridization with telomeric, 5S, and 28S rDNA probes) methods. We observed stability on both macro and micro-chromosomal levels. The diploid chromosome number was 2n = 44, and the karyotype was invariably composed of three pairs of meta/submetacentric and 19 pairs of subtelo/acrocentric chromosomes in all analysed species, with the same numbers of rDNA clusters and distribution of heterochromatin. The results suggest the evolutionary stability of chromosomal set; therefore, the large-scale chromosomal rearrangements seem to be unlikely associated with the sympatric speciation in Barombi Mbo.

The coincidence of ecological opportunity with hybridization explains rapid adaptive radiation in Lake Mweru cichlids

The coincidence of ecological opportunity with hybridization explains rapid adaptive radiation in Lake Mweru cichlids

Chance and predictability in evolution: The genomic basis of convergent dietary specializations in an adaptive radiation.

The coexistence of multiple eco-phenotypes in independently assembled communities makes island adaptive radiations the ideal framework to test convergence and parallelism in evolution. In the radiation of the spider genus Dysdera in the Canary Islands, species diversification occurs concomitant with repeated events of trophic specialization. These dietary shifts, to feed primarily on woodlice, are accompanied by modifications in morphology (mostly in the mouthparts), behaviour and nutritional physiology. To gain insight into the molecular basis of this adaptive radiation, we performed a comprehensive comparative transcriptome analysis of five Canary Island Dysdera endemics representing two evolutionary and geographically independent events of dietary specialization. After controlling for the potential confounding effects of hemiplasy, our differential gene expression and selective constraint analyses identified a number of genetic changes that could be associated with the repeated adaptations to specialized diet of woodlice, including some related to heavy metal detoxification and homeostasis, the metabolism of some important nutrients and venom toxins. Our results shed light on the genomic basis of an extraordinary case of dietary shift convergence associated with species diversification. We uncovered putative molecular substrates of convergent evolutionary changes at different hierarchical levels, including specific genes, genes with equivalent functions and even particular amino acid positions. This study improves our knowledge of rapid adaptive radiations and provides new insights into the predictability of evolution.

Host defense triggers rapid adaptive radiation in experimentally evolving parasites.

Adaptive radiation occurs when the members of a single lineage evolve different adaptive forms in response to selection imposed by competitors or predators. Iconic examples include Darwin's finches, Caribbean anoles, and Hawaiian silverswords, all of which live on islands. Although adaptive radiation is thought to be an important generator of biodiversity, most studies concern groups that have already diversified. Here, we take the opposite approach. We experimentally triggered diversification in the descendants of a single population of host‐specific parasites confined to different host “islands.” We show rapid adaptive divergence of experimentally evolving feather lice in response to preening, which is a bird's main defense against ectoparasites. We demonstrate that host defense exerts strong phenotypic selection for crypsis in lice transferred to different colored rock pigeons (Columba livia). During four years of experimental evolution (∼60 generations), the lice evolved heritable differences in color. Strikingly, the observed color differences spanned the range of phenotypes found among congeneric lice adapted to other species of birds. To our knowledge, this is the first real‐time demonstration that microevolution is fast enough to simulate millions of years of macroevolutionary change. Our results further indicate that host‐mediated selection triggers rapid divergence in the adaptive radiation of parasites, which are among the most diverse organisms on Earth.

Evolutionary Comparison of the Chloroplast Genome in the Woody Sonchus Alliance (Asteraceae) on the Canary Islands.

The woody Sonchus alliance consists primarily of woody species of the genus Sonchus (subgenus Dendrosonchus; family Asteraceae). Most members of the alliance are endemic to the oceanic archipelagos in the phytogeographic region of Macaronesia. They display extensive morphological, ecological, and anatomical diversity, likely caused by the diverse habitats on islands and rapid adaptive radiation. As a premier example of adaptive radiation and insular woodiness of species endemic to oceanic islands, the alliance has been the subject of intensive evolutionary studies. While phylogenetic studies suggested that it is monophyletic and its major lineages radiated rapidly early in the evolutionary history of this group, genetic mechanisms of speciation and genomic evolution within the alliance remain to be investigated. We first attempted to address chloroplast (cp) genome evolution by conducting comparative genomic analysis of three representative endemic species (Sonchus acaulis, Sonchus canariensis, and Sonchus webbii) from the Canary Islands. Despite extensive morphological, anatomical, and ecological differences among them, their cp genomes were highly conserved in gene order and content, ranging from 152,071 to 152,194 bp in total length. The number of repeat variations and six highly variable regions were identified as valuable molecular markers. Phylogenetic analysis of 32 species in the family Asteraceae revealed the phylogenetic position of the woody Sonchus alliance within the tribe Cichorieae and the sister relationship between the weedy Sonchus oleraceus and the alliance.

Rapid Divergence Followed by Adaptation to Contrasting Ecological Niches of Two Closely Related Columbine Species Aquilegia japonica and A. oxysepala.

Elucidating the mechanisms underlying the genetic divergence between closely related species is crucial to understanding the origin and evolution of biodiversity. The genus Aquilegia L. has undergone rapid adaptive radiation, generating about 70 well-recognized species that are specialized to distinct habitats and pollinators. In this study, to address the underlying evolutionary mechanisms that drive the genetic divergence, we analyzed the whole genomes of two ecologically isolated Aquilegia species, A. oxysepala and A. japonica as well as their putative hybrid. Our comparative genomic analyses reveal that while the two species diverged only recently and experienced recurrent gene flow, a high level of genetic divergence is observed in their nuclear genomes. In particular, candidate genomic regions that show signature of selection differ dramatically between the two species. Given that the splitting time of the two species is broadly matched with the decrease in effective population sizes, we propose that allopatric isolation together with natural selection have preceded the interspecific gene flow in the process of speciation. The observed high genetic divergence is likely an outcome of combined effects of natural selection, genetic drift and divergent sorting of ancestral polymorphisms. Our study provides a genome-wide view of how genetic divergence has evolved between closely related species.

Recent lake expansion triggered the adaptive radiation of freshwater snails in the ancient Lake Biwa.

Lake expansion that leads to the formation of new habitats has potential to drive intralacustrine diversification. The ancient Lake Biwa in central Japan has historically experienced substantial changes in the lake size, and it provides a useful system for evaluating the role of lake‐size fluctuations in the diversification of endemic fauna. Here, we used genome‐wide DNA analyses and reconstructed the diversification history of the endemic freshwater snails belonging to the subgenus Biwamelania with respect to the geological history of Lake Biwa. We found that two genetically distinct snail lineages independently colonized Lake Biwa and they concurrently and rapidly radiated into 15 extant Biwamelania species. A combination of paleontological evidence and molecular dating technique demonstrated that the radiation of Biwamelania was tightly linked to the latest enlargement of the lake about 0.4 million years ago and suggested that increased ecological opportunity associated with the lake expansion drove the rapid adaptive radiation. We propose that the Biwamelania snails in Lake Biwa offer a promising new system for understanding the association between the geological history of the lake and rapid intralacustrine diversification.

Changing Ecological Opportunities Facilitated the Explosive Diversification of New Caledonian Oxera (Lamiaceae).

Phylogenies recurrently demonstrate that oceanic island systems have been home to rapid clade diversification and adaptive radiations. The existence of adaptive radiations posits a central role of natural selection causing ecological divergence and speciation, and some plant radiations have been highlighted as paradigmatic examples of such radiations. However, neutral processes may also drive speciation during clade radiations, with ecological divergence occurring following speciation. Here, we document an exceptionally rapid and unique radiation of Lamiaceae within the New Caledonian biodiversity hotspot. Specifically, we investigated various biological, ecological, and geographical drivers of species diversification within the genus Oxera. We found that Oxera underwent an initial process of rapid cladogenesis likely triggered by a dramatic period of aridity during the early Pliocene. This early diversification of Oxera was associated with an important phase of ecological diversification triggered by significant shifts of pollination syndromes, dispersal modes, and life forms. Finally, recent diversification of Oxera appears to have been further driven by the interplay of allopatry and habitat shifts likely related to climatic oscillations. This suggests that Oxera could be regarded as an adaptive radiation at an early evolutionary stage that has been obscured by more recent joint habitat diversification and neutral geographical processes. Diversification within Oxera has perhaps been triggered by varied ecological and biological drivers acting in a leapfrog pattern, but geographic processes may have been an equally important driver. We suspect that strictly adaptive radiations may be rare in plants and that most events of rapid clade diversification may have involved a mixture of geographical and ecological divergence.

Rapid Pliocene adaptive radiation of modern kangaroos.

Differentiating between ancient and younger, more rapidly evolved clades is important for determining paleoenvironmental drivers of diversification. Australia possesses many aridity-adapted lineages, the origins of which have been closely linked to late Miocene continental aridification. Using dental macrowear and molar crown height measurements, spanning the past 25 million years, we show that the most iconic Australian terrestrial mammals, "true" kangaroos (Macropodini), adaptively radiated in response to mid-Pliocene grassland expansion rather than Miocene aridity. In contrast, low-crowned, short-faced kangaroos radiated into predominantly browsing niches as the late Cenozoic became more arid, contradicting the view that this was an interval of global browser decline. Our results implicate warm-to-cool climatic oscillations as a trigger for adaptive radiation and refute arguments attributing Pleistocene megafaunal extinction to aridity-forced dietary change.

Unravelling relationships among the shared stripes of sailors: Mitogenomic phylogeny of Limenitidini butterflies (Lepidoptera, Nymphalidae, Limenitidinae), focusing on the genera Athyma and Limenitis

The phylogenetic relationships of the nymphalid butterfly tribe Limenitidini are best known for the genera Limenitis and Adelpha, model taxa for evolutionary processes such as Batesian mimicry and rapid adaptive radiations. Whereas these American limenitidines have received the most attention, phylogenetic relationships of their Asian relatives are still controversial and largely unexplored. Even one of the largest genera in Asia, Athyma, is polyphyletic. To clarify the phylogenetic relationships of these Asian Limenitidini, a total of 53 representatives were sampled; 37 have their mitogenomes sequenced for the first time. Our phylogenetic results confirm that mitogenomic data provides well-resolved relationships at most major levels of the phylogeny, even using different partition schemes or different inference methods. Interestingly, our results show that some Athyma taxa are embedded within the genus Limenitis, whereas the genus Tacola, previously considered to be a synonym of Athyma, needs to be recognized as a valid clade. Additionally, the other Limenitidini genera in Asia (namely Tarattia, Litinga, Sumalia, Pandita and Patsuia) are now grouped either within Athyma or Limenitis, so these genera need to be sunk. Importantly, we also show that the mainly Old World Limenitis and entirely New World Adelpha are sister groups, confirming the relevance of Asian lineages to global studies of Limenitis evolution.

Hybridization can promote adaptive radiation by means of transgressive segregation.

Understanding the mechanisms of rapid adaptive radiation has been a central problem of evolutionary ecology. Recently, there is a growing recognition that hybridization between different evolutionary lineages can facilitate adaptive radiation by creating novel phenotypes. Yet, theoretical plausibility of this hypothesis remains unclear because, for example, hybridization can negate pre-existing species richness. Here, we theoretically investigate whether and under what conditions hybridization promotes ecological speciation and adaptive radiation using an individual-based model to simulate genome evolution following hybridization between two allopatrically evolved lineages. The model demonstrated that transgressive segregation through hybridization can facilitate adaptive radiation, most powerfully when novel vacant ecological niches are highly dissimilar, phenotypic effect size of mutations is small and there is moderate genetic differentiation between parental lineages. These results provide a theoretical basis for the effect of hybridization facilitating adaptive radiation.

Molecular investigation of genetic assimilation during the rapid adaptive radiations of East African cichlid fishes.

Adaptive radiations are characterized by adaptive diversification intertwined with rapid speciation within a lineage resulting in many ecologically specialized, phenotypically diverse species. It has been proposed that adaptive radiations can originate from ancestral lineages with pronounced phenotypic plasticity in adaptive traits, facilitating ecologically driven phenotypic diversification that is ultimately fixed through genetic assimilation of gene regulatory regions. This study aimed to investigate how phenotypic plasticity is reflected in gene expression patterns in the trophic apparatus of several lineages of East African cichlid fishes, and whether the observed patterns support genetic assimilation. This investigation used a split brood experimental design to compare adaptive plasticity in species from within and outside of adaptive radiations. The plastic response was induced in the crushing pharyngeal jaws through feeding individuals either a hard or soft diet. We find that nonradiating, basal lineages show higher levels of adaptive morphological plasticity than the derived, radiated lineages, suggesting that these differences have become partially genetically fixed during the formation of the adaptive radiations. Two candidate genes that may have undergone genetic assimilation, gif and alas1, were identified, in addition to alterations in the wiring of LPJ patterning networks. Taken together, our results suggest that genetic assimilation may have dampened the inducibility of plasticity related genes during the adaptive radiations of East African cichlids, flattening the reaction norms and canalizing their feeding phenotypes, driving adaptation to progressively more narrow ecological niches.