High levels of interspecific gene flow in an endemic cichlid fish adaptive radiation from an extreme lake environment

Studying recent adaptive radiations in isolated insular systems avoids complicating causal events and thus may offer clearer insight into mechanisms generating biological diversity. Here, we investigate evolutionary relationships and genomic differentiation within the recent radiation of Alcolapia cichlid fish that exhibit extensive phenotypic diversification, and which are confined to the extreme soda lakes Magadi and Natron in East Africa. We generated an extensive RAD data set of 96 individuals from multiple sampling sites and found evidence for genetic admixture between species within Lake Natron, with the highest levels of admixture between sympatric populations of the most recently diverged species. Despite considerable environmental separation, populations within Lake Natron do not exhibit isolation by distance, indicating panmixia within the lake, although individuals within lineages clustered by population in phylogenomic analysis. Our results indicate exceptionally low genetic differentiation across the radiation despite considerable phenotypic trophic variation, supporting previous findings from smaller data sets; however, with the increased power of densely sampled SNPs, we identify genomic peaks of differentiation (F_ST outliers) between Alcolapia species. While evidence of ongoing gene flow and interspecies hybridization in certain populations suggests that Alcolapia species are incompletely reproductively isolated, the identification of outlier SNPs under diversifying selection indicates the radiation is undergoing adaptive divergence.     

Plasticity paves the way in an adaptive radiation

Phenotypic plasticity has been hypothesized to play a central role in the evolution of phenotypic diversity across species (West‐Eberhard 2003 ). Through ‘genetic assimilation’, phenotypes that are initially environmentally induced within species become genetically fixed over evolutionary time. While genetic assimilation has been shown to occur in both the laboratory and the field (Waddington 1953 ; Aubret & Shine 2009 ), it remains to be shown whether it can account for broad patterns of phenotypic diversity across entire adaptive radiations. Furthermore, our ignorance of the underlying molecular mechanisms has hampered our ability to incorporate phenotypic plasticity into models of evolutionary processes. In this issue of Molecular Ecology, Parsons et al. ( 2016 ) take a significant step in filling these conceptual gaps making use of cichlid fishes as a powerful study system. Cichlid jaw and skull morphology show adaptive, plastic changes in response to early dietary experiences (Fig. 1). In this research, Parsons et al. ( 2016 ) first show that the direction of phenotypic plasticity aligns with the major axis of phenotypic divergence across species. They then dissect the underlying genetic architecture of this plasticity, showing that it is specific to the developmental environment and implicating the patched locus in genetic assimilation (i.e. a reduction in the environmental sensitivity of that locus in the derived species).     

Allopatric and sympatric diversification within roach (Rutilus rutilus) of large pre‐alpine lakes

Intraspecific differentiation in response to divergent natural selection between environments is a common phenomenon in some northern freshwater fishes, especially salmonids and stickleback. Understanding why these taxa diversify and undergo adaptive radiations while most other fish species in the same environments do not, remains an open question. The possibility for intraspecific diversification has rarely been evaluated for most northern freshwater fish species. Here, we assess the potential for intraspecific differentiation between and within lake populations of roach (Rutilus rutilus)—a widespread and abundant cyprinid species—in lakes in which salmonids have evolved endemic adaptive radiations. Based on more than 3,000 polymorphic RADseq markers, we detected low but significant genetic differentiation between roach populations of two ultraoligotrophic lakes and between these and populations from other lakes. This, together with differentiation in head morphology and stable isotope signatures, suggests evolutionary and ecological differentiation among some of our studied populations. Next, we tested for intralacustrine diversification of roach within Lake Brienz, the most pristine lake surveyed in this study. We found significant phenotypic evidence for ecological intralacustrine differentiation between roach caught over a muddy substrate and those caught over a rocky substrate. However, evidence for intralacustrine genetic differentiation is at best subtle and phenotypic changes may therefore be mostly plastic. Overall, our findings suggest roach can differ between ecologically distinct lakes, but the extent of intralacustrine ecological differentiation is weak, which contrasts with the strong differentiation among endemic species of whitefish in the same lakes.     

SPECIES‐SPECIFIC DIFFERENCES IN ADAPTIVE PHENOTYPIC PLASTICITY IN AN ECOLOGICALLY RELEVANT TROPHIC TRAIT: HYPERTROPHIC LIPS IN MIDAS CICHLID FISHES

The spectacular species richness of cichlids and their diversity in morphology, coloration, and behavior have made them an ideal model for the study of speciation and adaptive evolution. Hypertrophic lips evolved repeatedly and independently in African and Neotropical cichlid radiations. Cichlids with hypertrophic lips forage predominantly in rocky crevices and it has been hypothesized that mechanical stress caused by friction could result in larger lips through phenotypic plasticity. To test the influence of the environment on the size and development of lips, we conducted a series of breeding and feeding experiments on Midas cichlids. Full‐sibs of Amphilophus labiatus (thick‐lipped) and Amphilophus citrinellus (thin‐lipped) each were split into a control group which was fed food from the water column and a treatment group whose food was fixed to substrates. We found strong evidence for phenotypic plasticity on lip area in the thick‐lipped species, but not in the thin‐lipped species. Intermediate phenotypic values were observed in hybrids from thick‐ and thin‐lipped species reared under “control” conditions. Thus, both a genetic, but also a phenotypic plastic component is involved in the development of hypertrophic lips in Neotropical cichlids. Moreover, species‐specific adaptive phenotypic plasticity was found, suggesting that plasticity is selected for in recent thick‐lipped species.     

Change in sexual signalling traits outruns morphological divergence across an ecological gradient in the post‐glacial radiation of the songbird genus Junco

The relative roles of natural and sexual selection in promoting evolutionary lineage divergence remains controversial and difficult to assess in natural systems. Local adaptation through natural selection is known to play a central role in promoting evolutionary divergence, yet secondary sexual traits can vary widely among species in recent radiations, suggesting that sexual selection may also be important in the early stages of speciation. Here, we compare rates of divergence in ecologically relevant traits (morphology) and sexually selected signalling traits (coloration) relative to neutral structure in genome‐wide molecular markers and examine patterns of variation in sexual dichromatism to explore the roles of natural and sexual selection in the diversification of the songbird genus Junco (Aves: Passerellidae). Juncos include divergent lineages in Central America and several dark‐eyed junco (J. hyemalis) lineages that diversified recently as the group recolonized North America following the last glacial maximum (ca. 18,000 years ago). We found an accelerated rate of divergence in sexually selected characters relative to ecologically relevant traits. Moreover, sexual dichromatism measurements suggested a positive relationship between the degree of colour divergence and the strength of sexual selection when controlling for neutral genetic distance. We also found a positive correlation between dichromatism and latitude, which coincides with the geographic axis of decreasing lineage age in juncos but also with a steep ecological gradient. Finally, we found significant associations between genome‐wide variants linked to functional genes and proxies of both sexual and natural selection. These results suggest that the joint effects of sexual and ecological selection have played a prominent role in the junco radiation.     

Adaptive phenotypic plasticity contributes to divergence between lake and river populations of an East African cichlid fish

Adaptive phenotypic plasticity and fixed genotypic differences have long been considered opposing strategies in adaptation. More recently, these mechanisms have been proposed to act complementarily and under certain conditions jointly facilitate evolution, speciation, and even adaptive radiations. Here, we investigate the relative contributions of adaptive phenotypic plasticity vs. local adaptation to fitness, using an emerging model system to study early phases of adaptive divergence, the generalist cichlid fish species Astatotilapia burtoni. We tested direct fitness consequences of morphological divergence between lake and river populations in nature by performing two transplant experiments in Lake Tanganyika. In the first experiment, we used wild‐caught juvenile lake and river individuals, while in the second experiment, we used F1 crosses between lake and river fish bred in a common garden setup. By tracking the survival and growth of translocated individuals in enclosures in the lake over several weeks, we revealed local adaptation evidenced by faster growth of the wild‐caught resident population in the first experiment. On the other hand, we did not find difference in growth between different types of F1 crosses in the second experiment, suggesting a substantial contribution of adaptive phenotypic plasticity to increased immigrant fitness. Our findings highlight the value of formally comparing fitness of wild‐caught and common garden‐reared individuals and emphasize the necessity of considering adaptive phenotypic plasticity in the study of adaptive divergence.     

Where Am I? Niche constraints due to morphological specialization in two Tanganyikan cichlid fish species

Food resource specialization within novel environments is considered a common axis of diversification in adaptive radiations. Feeding specializations are often coupled with striking morphological adaptations and exemplify the relation between morphology and diet (phenotype–environment correlations), as seen in, for example, Darwin finches, Hawaiian spiders, and the cichlid fish radiations in East African lakes. The cichlids' potential to rapidly exploit and occupy a variety of different habitats has previously been attributed to the variability and adaptability of their trophic structures including the pharyngeal jaw apparatus. Here we report a reciprocal transplant experiment designed to explore the adaptability of the trophic structures in highly specialized cichlid fish species. More specifically, we forced two common but ecologically distinct cichlid species from Lake Tanganyika, Tropheus moorii (rock‐dweller), and Xenotilapia boulengeri (sand‐dweller), to live on their preferred as well as on an unpreferred habitat (sand and rock, respectively). We measured their overall performance on the different habitat types and explored whether adaptive phenotypic plasticity is involved in adaptation. We found that, while habitat had no effect on the performance of X. boulengeri, T. moorii performed significantly better in its preferred habitat. Despite an experimental duration of several months, we did not find a shift in the morphology of the lower pharyngeal jaw bone that would be indicative of adaptive phenotypic plasticity in this trait.     

Habitat‐driven diversification,hybridization and cryptic diversity in the Fork‐tailed Drongo (Passeriformes: Dicruridae: Dicrurus adsimilis)

Species complexes of widespread African vertebrates that include taxa distributed across different habitats are poorly understood in terms of their phylogenetic relationships, levels of genetic differentiation and diversification dynamics. The Fork‐tailed Drongo (Dicrurus adsimilis) species complex includes seven Afrotropical taxa with parapatric distributions, each inhabiting a particular bioregion. Various taxonomic hypotheses concerning the species limits of the Fork‐tailed Drongo have been suggested, based largely on mantle and upperpart coloration, but our understanding of diversity and diversification patterns remains incomplete. Especially given our lack of knowledge about how well these characters reflect taxonomy in a morphologically conservative group. Using a thorough sampling across Afrotropical bioregions, we suggest that the number of recognized species within the D. adsimilis superspecies complex has likely been underestimated and that mantle and upperpart coloration reflects local adaptation to different habitat structure, rather than phylogenetic relationships. Our results are consistent with recent phylogeographic studies of sub‐Saharan African vertebrates, indicating that widespread and often morphologically uniform species comprise several paraphyletic lineages, often with one or more of the lineages being closely related to phenotypically distinct forms inhabiting a different, yet geographically close, biome.     

Inbreeding and adaptive plasticity: an experimental analysis on predator‐induced responses in the water flea Daphnia

Several studies have emphasized that inbreeding depression (ID) is enhanced under stressful conditions. Additionally, one might imagine a loss of adaptively plastic responses which may further contribute to a reduction in fitness under environmental stress. Here, we quantified ID in inbred families of the cyclical parthenogen Daphnia magna in the absence and presence of fish predation risk. We test whether predator stress affects the degree of ID and if inbred families have a reduced capacity to respond to predator stress by adaptive phenotypic plasticity. We obtained two inbred families through clonal selfing within clones isolated from a fish pond. After mild purging under standardized conditions, we compared life history traits and adaptive plasticity between inbred and outbred lineages (directly hatched from the natural dormant egg bank of the same pond). Initial purging of lineages under standardized conditions differed among inbred families and exceeded that in outbreds. The least purged inbred family exhibited strong ID for most life history traits. Predator‐induced stress hardly affected the severity of ID, but the degree to which the capacity for adaptive phenotypic plasticity was retained varied strongly among the inbred families. The least purged family overall lacked the capacity for adaptive phenotypic plasticity, whereas the family that suffered only mild purging exhibited a potential for adaptive plasticity that was comparable to the outbred population. We thus found that inbred offspring may retain the capacity to respond to the presence of fish by adaptive phenotypic plasticity, but this strongly depends on the parental clone engaging in selfing.     

Parallel adaptation to climate above the 35th parallel

Independent or parallel evolution of similar traits is key to understanding the genetics and limitations of adaptation. Adaptation from the same genetic changes in different populations defines parallel evolution. Such genetic changes can derive from standing ancestral variation or de novo mutations and excludes instances of adaptive introgression. In this issue of Molecular Ecology, Walden et al.(2020) investigate the scale of parallel climate adaptation from standing genetic variation between two North American Arabidopsis lyrata lineages, each formed by a distinct evolutionary history during the last glacial cycle. By identifying adaptive variants correlated with three ecologically significant climatic gradients, they show that instead of the same genetic variants or even genes, parallel evolution is only observed at the level of biological processes. The evolution of independent adaptive variants to climate in two genetically close lineages is explained by their different post‐glacial demographic histories. Separate glacial refugia and strong population bottlenecks were probably sufficient to change the landscape of shared allele frequencies, hindering the possibility of parallel evolution.     

Evidence for ecological speciation via a host shift in the holly leaf miner,Phytomyza glabricola (Diptera: Agromyzidae)

Evolutionary radiations have been well documented in plants and insects, and natural selection may often underly these radiations. If radiations are adaptive, the diversity of species could be due to ecological speciation in these lineages. Agromyzid flies exhibit patterns of repeated host‐associated radiations. We investigated whether host‐associated population divergence and evidence of divergent selection exist in the leaf miner Phytomyza glabricola on its sympatric host plants, the holly species, Ilex coriacea and I. glabra. Using AFLPs and nuclear sequence data, we found substantial genetic divergence between host‐associated populations of these flies throughout their geographic range. Genome scans using the AFLP data identified 13 loci under divergent selection, consistent with processes of ecological speciation. EF‐1α data suggest that I. glabra is the original host of P. glabricola and that I. coriacea is the novel host, but the AFLP data are ambiguous with regard to directionality of the host shift.     

Rapid lineage accumulation in a non-adaptive radiation: phylogenetic analysis of diversification rates in eastern North American woodland salamanders (Plethodontidae: Plethodon)

Adaptive radiations have served as model systems for quantifying the build-up of species richness. Few studies have quantified the tempo of diversification in species-rich clades that contain negligible adaptive disparity, making the macroevolutionary consequences of different modes of evolutionary radiation difficult to assess. We use mitochondrial-DNA sequence data and recently developed phylogenetic methodologies to explore the tempo of diversification of eastern North American Plethodon, a species-rich clade of woodland salamanders exhibiting only limited phenotypic disparity. Lineage-through-time analysis reveals a high rate of lineage accumulation, 0.8 species per million years, occurring 11-8 million years ago in the P. glutinosus species group, followed by decreasing rates. This high rate of lineage accumulation is exceptional, comparable to the most rapid of adaptive radiations. In contrast to classic models of adaptive radiation where ecological niche divergence is linked to the origin of species, we propose that phylogenetic niche conservatism contributes to the rapid accumulation of P. glutinosus-group lineages by promoting vicariant isolation and multiplication of species across a spatially and temporally fluctuating environment. These closely related and ecologically similar lineages persist through long-periods of evolutionary time and form strong barriers to the geographic spread of their neighbours, producing a subsequent decline in lineage accumulation. Rapid diversification among lineages exhibiting long-term maintenance of their bioclimatic niche requirements is an under-appreciated phenomenon driving the build-up of species richness.     

A preliminary classification of evolutionary radiations

Rapid increases in taxonomic diversity are generally described as adaptive or evolutionary radiations. Such radiations differ widely in the rate and extent of morphologic innovation, taxonomic diversification and phylogenetic breadth, suggesting that several patterns, and likely processes, are involved. At least four distinct patterns of evolutionary radiation can be identified: novelty events, which generate new morphological complexity (altering the body plan of the group under consideration) but not necessarily with the associated production of many lower taxa; broad diversification events involving many independent lineages that undergo diversification, generate many new species and are driven by new ecological opportunities; economic radiations of a limited group of ecologically (but not necessarily phylogenetically) related clades exploiting a limited new ecologic opportunity; and adaptive radiations that may occur at any taxonomic level, but involve a rapid increase in diversity within a single clade, including “true”; adaptive radiations. Many events produce simple diversity increases with no corresponding increase in genetic/developmental/morphological/behavioral sophistication, but the most evolutionarily interesting events add new levels of complexity.     

Patterns of morphological variation among populations of the widespread annual killifish Nothobranchius orthonotus are independent of genetic divergence and biogeography

Populations of annual killifish of the genus Nothobranchius occur in patchily distributed temporary pools in the East African savannah. Their fragmented distribution and low dispersal ability result in highly structured genetic clustering of their populations. In this study, we examined body shape variation in a widely distributed species, Nothobranchius orthonotus with known phylogeographic structure. We tested whether genetic divergence of major mitochondrial lineages forming two candidate species is congruent with phenotypic diversification, using linear and geometric morphometry analyses of body shape in 23 wild populations. We also conducted a common‐garden experiment with two wild‐derived populations to control for the effect of local environmental conditions on body shape. We identified different allometric trajectories for different mitochondrial lineages and candidate species in both sexes. However, in a principal components analysis of population‐level body shape, the separation among mitochondrial lineages was incomplete. Higher similarity of mitochondrial lineages belonging to different candidate species than that of same candidate species prevented distinction of the two candidate species on the basis of body shape. Analysis at the individual level demonstrated that N. orthonotus express high intrapopulation variability, with major overlap among individuals from all populations. In conclusion, we suggest that N. orthonotus be considered as a single species with an extensive geographic range, strong population genetic structure and high morphological variability.     

HOST‐SPECIALIST LINEAGES DOMINATE THE ADAPTIVE RADIATION OF REEF CORAL ENDOSYMBIONTS

Bursts in species diversification are well documented among animals and plants, yet few studies have assessed recent adaptive radiations of eukaryotic microbes. Consequently, we examined the radiation of the most ecologically dominant group of endosymbiotic dinoflagellates found in reef‐building corals, Symbiodinium Clade C, using nuclear ribosomal (ITS2), chloroplast (psbA^ncr), and multilocus microsatellite genotyping. Through a hierarchical analysis of high‐resolution genetic data, we assessed whether ecologically distinct Symbiodinium, differentiated by seemingly equivocal rDNA sequence differences, are independent species lineages. We also considered the role of host specificity in Symbiodinium speciation and the correspondence between endosymbiont diversification and Caribbean paleo‐history. According to phylogenetic, biological, and ecological species concepts, Symbiodinium Clade C comprises many distinct species. Although regional factors contributed to population‐genetic structuring of these lineages, Symbiodinium diversification was mainly driven by host specialization. By combining patterns of the endosymbiont's host specificity, water depth distribution, and phylogeography with paleo‐historical signals of climate change, we inferred that present‐day species diversity on Atlantic coral reefs stemmed mostly from a post‐Miocene adaptive radiation. Host‐generalist progenitors spread, specialized, and diversified during the ensuing epochs of prolonged global cooling and change in reef‐faunal assemblages. Our evolutionary reconstruction thus suggests that Symbiodinium undergoes “boom and bust” phases in diversification and extinction during major climate shifts.     

Rapid postglacial diversification and long‐term stasis within the songbird genus Junco: phylogeographic and phylogenomic evidence

Natural systems composed of closely related taxa that vary in the degree of phenotypic divergence and geographic isolation provide an opportunity to investigate the rate of phenotypic diversification and the relative roles of selection and drift in driving lineage formation. The genus Junco (Aves: Emberizidae) of North America includes parapatric northern forms that are markedly divergent in plumage pattern and colour, in contrast to geographically isolated southern populations in remote areas that show moderate phenotypic divergence. Here, we quantify patterns of phenotypic divergence in morphology and plumage colour and use mitochondrial DNA genes, a nuclear intron, and genomewide SNPs to reconstruct the demographic and evolutionary history of the genus to infer relative rates of evolutionary divergence among lineages. We found that geographically isolated populations have evolved independently for hundreds of thousands of years despite little differentiation in phenotype, in sharp contrast to phenotypically diverse northern forms, which have diversified within the last few thousand years as a result of the rapid postglacial recolonization of North America. SNP data resolved young northern lineages into reciprocally monophyletic lineages, indicating low rates of gene flow even among closely related parapatric forms, and suggesting a role for strong genetic drift or multifarious selection acting on multiple loci in driving lineage divergence. Juncos represent a compelling example of speciation in action, where the combined effects of historical and selective factors have produced one of the fastest cases of speciation known in vertebrates.     

Deep divergence among mitochondrial lineages in African jackals

Recently, molecular analyses revealed that African and Eurasian golden jackals are distinct species. This finding suggests re‐investigation of the phylogenetic relationships and taxonomy of other African members of the Canidae. Here, we provide a study on the phylogenetic relationship between populations of African jackals Lupulella mesomelas and L. adusta inferred from 962 bp of the mitochondrial cytochrome b (cytb) gene. As expected from its disjunct distribution, with one population in eastern Africa and the other one in southern Africa, we found two mitochondrial lineages within L. mesomelas, which diverged about 2.5 million years ago (Ma). In contrast, in L. adusta with its more continuous distribution in sub‐Saharan Africa, we found only a shallower genetic diversification, with the exception of the West African population, which diverged around 1.4 Ma from the Central and East African populations. Both divergence ages are older than, for example the 1.1–0.9 million years between the grey wolf Canis lupus and the African golden wolf C. lupaster. One taxonomic implication of our findings might be that the two L. mesomelas populations warrant species status. However, genome‐wide data with adequate geographical sampling are needed to substantiate our results.     

AN ADAPTIVE RADIATION OF FROGS IN A SOUTHEAST ASIAN ISLAND ARCHIPELAGO

Living amphibians exhibit a diversity of ecologies, life histories, and species‐rich lineages that offers opportunities for studies of adaptive radiation. We characterize a diverse clade of frogs (Kaloula, Microhylidae) in the Philippine island archipelago as an example of an adaptive radiation into three primary habitat specialists or ecotypes. We use a novel phylogenetic estimate for this clade to evaluate the tempo of lineage accumulation and morphological diversification. Because species‐level phylogenetic estimates for Philippine Kaloula are lacking, we employ dense population sampling to determine the appropriate evolutionary lineages for diversification analyses. We explicitly take phylogenetic uncertainty into account when calculating diversification and disparification statistics and fitting models of diversification. Following dispersal to the Philippines from Southeast Asia, Kaloula radiated rapidly into several well‐supported clades. Morphological variation within Kaloula is partly explained by ecotype and accumulated at high levels during this radiation, including within ecotypes. We pinpoint an axis of morphospace related directly to climbing and digging behaviors and find patterns of phenotypic evolution suggestive of ecological opportunity with partitioning into distinct habitat specialists. We conclude by discussing the components of phenotypic diversity that are likely important in amphibian adaptive radiations.