Young Adaptive Radiations Research Articles

From microcosm to macrocosm: adaptive radiation of Darwin’s finches

Abstract In this Perspective we show the value of studying living organisms in the field to understand their history. Darwin’s finches are an iconic example of the early stages of speciation in a young adaptive radiation that produced 18 species in little more than a million years. The question they pose is how and why so many species originated and diversified rapidly. A long-term study of four species of finches on the small island of Daphne Major, combined with genomic investigations, provide some answers in terms of extrinsic and intrinsic factors. Beak size and shape, as well as body size, are key heritable features involved in both ecological and reproductive isolation, and their evolution by natural selection was caused by competitor species during prolonged droughts. Introgressive hybridization of related species is rare but recurring, apparently widespread, increases genetic variation, and does not incur a fitness cost. Hybridization can produce a new species. We use a phylogeny based on whole genome sequences of the four finches to infer morphological transitions in their radiation. Several lines of evidence indicate that some species are missing from the early phase of the radiation due to extinction. Combining these results, we re-cast the classical allopatry-then-sympatry theory of adaptive radiation as a competition-selection-hybridization process that generates a diversity of species.

Ecological disturbance reduces genomic diversity across an Alpine whitefish adaptive radiation.

Genomic diversity is associated with the adaptive potential of a population and thereby impacts the extinction risk of a species during environmental change. However, empirical data on genomic diversity of populations before environmental perturbations are rare and hence our understanding of the impact of perturbation on diversity is often limited. We here assess genomic diversity utilising whole-genome resequencing data from all four species of the Lake Constance Alpine whitefish radiation. Our data covers a period of strong but transient anthropogenic environmental change and permits us to track changes in genomic diversity in all species over time. Genomic diversity became strongly reduced during the period of anthropogenic disturbance and has not recovered yet. The decrease in genomic diversity varies between 18% and 30%, depending on the species. Interspecific allele frequency differences of SNPs located in potentially ecologically relevant genes were homogenized over time. This suggests that in addition to the reduction of genome-wide genetic variation, the differentiation that evolved in the process of adaptation to alternative ecologies between species might have been lost during the ecological disturbance. The erosion of substantial amounts of genomic variation within just a few generations in combination with the loss of potentially adaptive genomic differentiation, both of which had evolved over thousands of years, demonstrates the sensitivity of biodiversity in evolutionary young adaptive radiations towards environmental disturbance. Natural history collections, such as the one used for this study, are instrumental in the assessment of genomic consequences of anthropogenic environmental change. Historical samples enable us to document biodiversity loss against the shifting baseline syndrome and advance our understanding of the need for efficient biodiversity conservation on a global scale.

Genetic architecture of adaptive radiation across two trophic levels.

Evolution of trophic diversity is a hallmark of adaptive radiation. Yet, transitions between carnivory and herbivory are rare in young adaptive radiations. Haplochromine cichlid fish of the African Great Lakes are exceptional in this regard. Lake Victoria was colonized by an insectivorous generalist and in less than 20 000 years, several clades of specialized herbivores evolved. Carnivorous versus herbivorous lifestyles in cichlids require many different adaptations in functional morphology, physiology and behaviour. Ecological transitions in either direction thus require many traits to change in a concerted fashion, which could be facilitated if genomic regions underlying these traits were physically linked or pleiotropic. However, linkage/pleiotropy could also constrain evolvability. To investigate components of the genetic architecture of a suite of traits that distinguish invertivores from algae scrapers, we performed quantitative trait locus (QTL) mapping using a second-generation hybrid cross. While we found indications of linkage/pleiotropy within trait complexes, QTLs for distinct traits were distributed across several unlinked genomic regions. Thus, a mixture of independently segregating variation and some pleiotropy may underpin the rapid trophic transitions. We argue that the emergence and maintenance of associations between the different genomic regions underpinning co-adapted traits that evolved and persist against some gene flow required reproductive isolation.

Benefits and limitations of a new genome-based PCR-RFLP genotyping assay (GB-RFLP): A SNP-based detection method for identification of species in extremely young adaptive radiations.

High‐throughput DNA sequencing technologies make it possible now to sequence entire genomes relatively easily. Complete genomic information obtained by whole‐genome resequencing (WGS) can aid in identifying and delineating species even if they are extremely young, cryptic, or morphologically difficult to discern and closely related. Yet, for taxonomic or conservation biology purposes, WGS can remain cost‐prohibitive, too time‐consuming, and often constitute a “data overkill.” Rapid and reliable identification of species (and populations) that is also cost‐effective is made possible by species‐specific markers that can be discovered by WGS. Based on WGS data, we designed a PCR restriction fragment length polymorphism (PCR‐RFLP) assay for 19 Neotropical Midas cichlid populations (Amphilophus cf. citrinellus), that includes all 13 described species of this species complex. Our work illustrates that identification of species and populations (i.e., fish from different lakes) can be greatly improved by designing genetic markers using available “high resolution” genomic information. Yet, our work also shows that even in the best‐case scenario, when whole‐genome resequencing information is available, unequivocal assignments remain challenging when species or populations diverged very recently, or gene flow persists. In summary, we provide a comprehensive workflow on how to design RFPL markers based on genome resequencing data, how to test and evaluate their reliability, and discuss the benefits and pitfalls of our approach.

Parallel and non-parallel changes of the gut microbiota during trophic diversification in repeated young adaptive radiations of sympatric cichlid fish

BackgroundRecent increases in understanding the ecological and evolutionary roles of microbial communities have underscored the importance of their hosts’ biology. Yet, little is known about gut microbiota dynamics during the early stages of ecological diversification and speciation. We sequenced the V4 region of the 16s rRNA gene to study the gut microbiota of Nicaraguan Midas cichlid fish (Amphilophus cf. citrinellus). Specifically, we tested the hypothesis that parallel divergence in trophic ecology in extremely young adaptive radiations from two crater lakes is associated with parallel changes of their gut microbiota.ResultsBacterial communities of fish guts and lake water were highly distinct, indicating that the gut microbiota is shaped by host-specific factors. Among individuals of the same crater lake, differentiation in trophic ecology was weakly associated with gut microbiota differentiation, suggesting that diet, to some extent, affects the gut microbiota. However, differences in trophic ecology were much more pronounced across than within species whereas similar patterns were not observed for taxonomic and functional differences of the gut microbiota. Across the two crater lakes, we could not detect conclusive evidence for parallel changes of the gut microbiota associated with trophic ecology.ConclusionsA lack of clearly differentiated niches during the early stages of ecological diversification might result in non-parallel changes of gut microbial communities, as observed in our study system as well as in other recently diverged fish species.2DLR1RhYgjPSYf_AZYrUvAVideo

The ecological and genomic basis of explosive adaptive radiation.

Speciation rates vary considerably among lineages, and our understanding of what drives the rapid succession of speciation events within young adaptive radiations remains incomplete1-11. The cichlid fish family provides a notable example of such variation, with many slowly speciating lineages as well as several exceptionallylarge and rapid radiations12. Here, by reconstructing a large phylogeny of all currently described cichlid species, we show that explosive speciation is solely concentrated in species flocks of several large young lakes. Increases in the speciation rate are associated with the absence of top predators; however, this does not sufficiently explain explosive speciation. Across lake radiations, we observe a positive relationship between the speciation rate and enrichment of large insertion or deletion polymorphisms. Assembly of 100 cichlid genomes within the most rapidly speciating cichlid radiation, which is found in Lake Victoria, reveals exceptional 'genomic potential'-hundreds of ancient haplotypes bear insertion or deletion polymorphisms, many of which are associated with specific ecologies and shared with ecologically similar species from other older radiations elsewhere in Africa. Network analysis reveals fundamentally non-treelike evolution through recombining old haplotypes, and the origins of ecological guilds are concentrated early in the radiation. Our results suggest that the combination of ecological opportunity, sexual selection and exceptional genomic potential is the key to understanding explosive adaptive radiation.

Triad hybridization via a conduit species

Introgressive hybridization can affect the evolution of populations in several important ways. It may retard or reverse divergence of species, enable the development of novel traits, enhance the potential for future evolution by elevating levels of standing variation, create new species, and alleviate inbreeding depression in small populations. Most of what is known of contemporary hybridization in nature comes from the study of pairs of species, either coexisting in the same habitat or distributed parapatrically and separated by a hybrid zone. More rarely, three species form an interbreeding complex (triad), reported in vertebrates, insects, and plants. Often, one species acts as a genetic link or conduit for the passage of genes (alleles) between two others that rarely, if ever, hybridize. Demographic and genetic consequences are unknown. Here we report results of a long-term study of interbreeding Darwin's finches on Daphne Major island, Galápagos. Geospiza fortis acted as a conduit for the passage of genes between two others that have never been observed to interbreed on Daphne: Geospiza fuliginosa, a rare immigrant, and Geospiza scandens, a resident. Microsatellite gene flow from G. fortis into G. scandens increased in frequency during 30 y of favorable ecological conditions, resulting in genetic and morphological convergence. G. fortis, G. scandens, and the derived dihybrids and trihybrids experienced approximately equal fitness. Especially relevant to young adaptive radiations, where species differ principally in ecology and behavior, these findings illustrate how new combinations of genes created by hybridization among three species can enhance the potential for evolutionary change.

Diversification in trophic morphology and a mating signal are coupled in the early stages of sympatric divergence in crossbills

AbstractUnderstanding the mechanisms generating diversity in mating signals is critical to understanding the process of speciation. One mechanism of mating signal diversification occurs when phenotypes that experience divergent ecological selection also affect the production of mating signals, resulting in a coupling between ecological diversification and mating signal diversification. Here, we present evidence that rapid diversification in bill size has resulted in the diversification of some components of song structure in a young adaptive radiation of seed-eating finches (red crossbill, Loxia curvirostra complex). Specifically, we find that larger-billed ecotypes sing songs with lower minimum frequencies, lower syllable repetition rates and greater vocal deviation (i.e. lower performance) than smaller-billed ecotypes for pure tonal syllables. In contrast, bill size was not correlated with maximum frequency or frequency bandwidth, and we found no relationship between bill size and any song parameters in buzzy syllables. Furthermore, we found no evidence for a relationship between the degree of bill size divergence and the potential for song discrimination between sympatric ecotypes. Because bill size is correlated with some features of pure tonal syllables (which appear to be most important for courtship in crossbills) in crossbill song, our results suggest that there was an early-evolving link between ecological and mating signal diversification that may have influenced the rapid evolution of reproductive isolation between sympatric ecotypes.

Role of sexual imprinting in assortative mating and premating isolation in Darwin’s finches

Global biodiversity is being degraded at an unprecedented rate, so it is important to preserve the potential for future speciation. Providing for the future requires understanding speciation as a contemporary ecological process. Phylogenetically young adaptive radiations are a good choice for detailed study because diversification is ongoing. A key question is how incipient species become reproductively isolated from each other. Barriers to gene exchange have been investigated experimentally in the laboratory and in the field, but little information exists from the quantitative study of mating patterns in nature. Although the degree to which genetic variation underlying mate-preference learning is unknown, we provide evidence that two species of Darwin's finches imprint on morphological cues of their parents and mate assortatively. Statistical evidence of presumed imprinting is stronger for sons than for daughters and is stronger for imprinting on fathers than on mothers. In combination, morphology and species-specific song learned from the father constitute a barrier to interbreeding. The barrier becomes stronger the more the species diverge morphologically and ecologically. It occasionally breaks down, and the species hybridize. Hybridization is most likely to happen when species are similar to each other in adaptive morphological traits, e.g., body size and beak size and shape. Hybridization can lead to the formation of a new species reproductively isolated from the parental species as a result of sexual imprinting. Conservation of sufficiently diverse natural habitat is needed to sustain a large sample of extant biota and preserve the potential for future speciation.

Divergent parasite infections in sympatric cichlid species in Lake Victoria.

Parasitism has been proposed as a factor in host speciation, as an agent affecting coexistence of host species in species-rich communities and as a driver of post-speciation diversification. Young adaptive radiations of closely related host species of varying ecological and genomic differentiation provide interesting opportunities to explore interactions between patterns of parasitism, divergence and coexistence of sympatric host species. Here, we explored patterns in ectoparasitism in a community of 16 fully sympatric cichlid species at Makobe Island in Lake Victoria, a model system of vertebrate adaptive radiation. We asked whether host niche, host abundance or host genetic differentiation explains variation in infection patterns. We found significant differences in infections, the magnitude of which was weakly correlated with the extent of genomic divergence between the host species, but more strongly with the main ecological gradient, water depth. These effects were most evident with infections of Cichlidogyrus monogeneans, whereas the only host species with a strictly crevice-dwelling niche, Pundamilia pundamilia, deviated from the general negative relationship between depth and parasitism. In accordance with the Janzen-Connell hypothesis, we also found that host abundance tended to be positively associated with infections in some parasite taxa. Data on the Pundamilia sister species pairs from three other islands with variable degrees of habitat (crevice) specialization suggested that the lower parasite abundance of P.pundamilia at Makobe could result from both habitat specialization and the evolution of specific resistance. Our results support influences of host genetic differentiation and host ecology in determining infections in this diverse community of sympatric cichlid species.

Building trophic specializations that result in substantial niche partitioning within a young adaptive radiation.

Dietary partitioning often accompanies the increased morphological diversity seen during adaptive radiations within aquatic systems. While such niche partitioning would be expected in older radiations, it is unclear how significant morphological divergence occurs within a shorter time period. Here we show how differential growth in key elements of the feeding mechanism can bring about pronounced functional differences among closely related species. An incredibly young adaptive radiation of three Cyprinodon species residing within hypersaline lakes in San Salvador Island, Bahamas, has recently been described. Characterized by distinct head shapes, gut content analyses revealed three discrete feeding modes in these species: basal detritivory as well as derived durophagy and lepidophagy (scale-feeding). We dissected, cleared and stained, and micro-CT scanned species to assess functionally relevant differences in craniofacial musculoskeletal elements. The widespread feeding mode previously described for cyprinodontiforms, in which the force of the bite may be secondary to the requisite dexterity needed to pick at food items, is modified within both the scale specialist and the durophagous species. While the scale specialist has greatly emphasized maxillary retraction, using it to overcome the poor mechanical advantage associated with scale-eating, the durophage has instead stabilized the maxilla. In all species the bulk of the adductor musculature is composed of AM A1. However, the combined masses of both adductor mandibulae (AM) A1 and A3 in the scale specialist were five times that of the other species, showing the importance of growth in functional divergence. The scale specialist combines plesiomorphic jaw mechanisms with both a hypertrophied AM A1 and a slightly modified maxillary anatomy (with substantial functional implications) to generate a bite that is both strong and allows a wide range of motion in the upper jaw, two attributes that normally tradeoff mechanically. Thus, a significant feeding innovation (scale-eating, rarely seen in fishes) may evolve based largely on allometric changes in ancestral structures. Alternatively, the durophage shows reduced growth with foreshortened jaws that are stabilized by an immobile maxilla. Overall, scale specialists showed the most divergent morphology, suggesting that selection for scale-biting might be stronger or act on a greater number of traits than selection for either detritivory or durophagy. The scale specialist has colonized an adaptive peak that few lineages have climbed. Thus, heterochronic changes in growth can quickly produce functionally relevant change among closely related species.

Ecosystem size predicts eco-morphological variability in a postglacial diversification.

Identifying the processes by which new phenotypes and species emerge has been a long‐standing effort in evolutionary biology. Young adaptive radiations provide a model to study patterns of morphological and ecological diversification in environmental context. Here, we use the recent radiation (ca. 12k years old) of the freshwater fish Arctic charr (Salvelinus alpinus) to identify abiotic and biotic environmental factors associated with adaptive morphological variation. Arctic charr are exceptionally diverse, and in postglacial lakes there is strong evidence of repeated parallel evolution of similar morphologies associated with foraging. We measured head depth (a trait reflecting general eco‐morphology and foraging ecology) of 1,091 individuals across 30 lake populations to test whether fish morphological variation was associated with lake bathymetry and/or ecological parameters. Across populations, we found a significant relationship between the variation in head depth of the charr and abiotic environmental characteristics: positively with ecosystem size (i.e., lake volume, surface area, depth) and negatively with the amount of littoral zone. In addition, extremely robust‐headed phenotypes tended to be associated with larger and deeper lakes. We identified no influence of co‐existing biotic community on Arctic charr trophic morphology. This study evidences the role of the extrinsic environment as a facilitator of rapid eco‐morphological diversification.

Sympatric ecological divergence associated with a color polymorphism.

BackgroundColor polymorphisms are a conspicuous feature of many species and a way to address broad ecological and evolutionary questions. Three potential major evolutionary fates of color polymorphisms are conceivable over time: maintenance, loss, or speciation. However, the understanding of color polymorphisms and their evolutionary implications is frequently impaired by sex-linkage of coloration, unknown inheritance patterns, difficulties in phenotypic characterization, and a lack of evolutionary replicates. Hence, the role of color polymorphisms in promoting ecological and evolutionary diversification remains poorly understood. In this context, we assessed the ecological and evolutionary consequences of a color polymorphic study system that is not hampered by these restrictions: the repeated adaptive radiations of the gold/dark Midas cichlid fishes (the Amphilophus citrinellus species complex) from the great lakes and crater lakes of Nicaragua, Central America.ResultsWe conducted multi-trait morphological and ecological analyses from ten populations of this young adaptive radiation (<6,000 years old), which revealed sympatric ecological differentiation associated with the conspicuous binary (gold/dark) color polymorphism. Varying degrees of intraspecific ecological divergence were observed across the ten color morph pairs, but most pairs exhibited a consistently parallel ecological and evolutionary trajectory across populations. Specifically, gold Midas cichlids are frequently deeper-bodied, have more robust pharyngeal jaws, and feed at a lower trophic level compared to conspecific, sympatric dark individuals. A common garden experiment suggests there is a genetic correlation of color and eco-morphological traits.ConclusionsWe demonstrate unprecedented ecological and evolutionary consequences of color polymorphism in this adaptive radiation. Across the species complex, sympatric conspecific individuals differed in eco-morphology depending on color morph (gold/dark) and the axis of differentiation tended to be consistent across replicates. The consistent divergence across wild populations and the common garden experiment suggests that color is genetically correlated to ecology. Because Midas cichlids are known to mate color assortatively, the putative genetic correlation of this color polymorphism with an eco-morphological divergence suggests an innate potential to promote ecological and evolutionary divergence across this species complex. However, there are to date no examples of speciation based on color in this radiation, suggesting long-term maintenance of this color polymorphism.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-015-0192-7) contains supplementary material, which is available to authorized users.

Ecological speciation and phenotypic plasticity affect ecosystems

Phenotypic differences among closely related populations and species can cause contrasting effects on ecosystems; however, it is unknown whether such effects result from genetic divergence, phenotypic plasticity, or both. To test this, we reared sympatric limnetic and benthic species of whitefish from a young adaptive radiation in a common garden, where the benthic species was raised on two distinct food types. We then used these fish in a mesocosm experiment to test for contrasting ecosystem effects of closely related species and of plastically induced differences within a species. We found that strong contrasting ecosystem effects resulted more frequently from genetic divergence, although they were not stronger overall than those resulting from phenotypic plasticity. Overall, our results provide evidence that genetically based differences among closely related species that evolved during a young adaptive radiation can affect ecosystems, and that phenotypic plasticity can modify the ecosystem effects of such species.

Crater lake cichlids individually specialize along the benthic-limnetic axis.

A common pattern of adaptive diversification in freshwater fishes is the repeated evolution of elongated open water (limnetic) species and high-bodied shore (benthic) species from generalist ancestors. Studies on phenotype-diet correlations have suggested that population-wide individual specialization occurs at an early evolutionary and ecological stage of divergence and niche partitioning. This variable restricted niche use across individuals can provide the raw material for earliest stages of sympatric divergence. We investigated variation in morphology and diet as well as their correlations along the benthic-limnetic axis in an extremely young Midas cichlid species, Amphilophus tolteca, endemic to the Nicaraguan crater lake Asososca Managua. We found that A. tolteca varied continuously in ecologically relevant traits such as body shape and lower pharyngeal jaw morphology. The correlation of these phenotypes with niche suggested that individuals are specialized along the benthic-limnetic axis. No genetic differentiation within the crater lake was detected based on genotypes from 13 microsatellite loci. Overall, we found that individual specialization in this young crater lake species encompasses the limnetic-as well as the benthic macro-habitat. Yet there is no evidence for any diversification within the species, making this a candidate system for studying what might be the early stages preceding sympatric divergence.A common pattern of adaptive diversification in freshwater fishes is the repeated evolution of open water (limnetic) species and of shore (benthic) species. Individual specialization can reflect earliest stages of evolutionary and ecological divergence. We here demonstrate individual specialization along the benthic–limnetic axis in a young adaptive radiation of crater lake cichlid fishes.

Population genomic signatures of divergent adaptation, gene flow and hybrid speciation in the rapid radiation ofLakeVictoria cichlid fishes

Adaptive radiations are an important source of biodiversity and are often characterized by many speciation events in very short succession. It has been proposed that the high speciation rates in these radiations may be fuelled by novel genetic combinations produced in episodes of hybridization among the young species. The role of such hybridization events in the evolutionary history of a group can be investigated by comparing the genealogical relationships inferred from different subsets of loci, but such studies have thus far often been hampered by shallow genetic divergences, especially in young adaptive radiations, and the lack of genome-scale molecular data. Here, we use a genome-wide sampling of SNPs identified within restriction site-associated DNA (RAD) tags to investigate the genomic consistency of patterns of shared ancestry and adaptive divergence among five sympatric cichlid species of two genera, Pundamilia and Mbipia, which form part of the massive adaptive radiation of cichlids in the East African Lake Victoria. Species pairs differ along several axes: male nuptial colouration, feeding ecology, depth distribution, as well as the morphological traits that distinguish the two genera and more subtle morphological differences. Using outlier scan approaches, we identify signals of divergent selection between all species pairs with a number of loci showing parallel patterns in replicated contrasts either between genera or between male colour types. We then create SNP subsets that we expect to be characterized to different extents by selection history and neutral processes and describe phylogenetic and population genetic patterns across these subsets. These analyses reveal very different evolutionary histories for different regions of the genome. To explain these results, we propose at least two intergeneric hybridization events (between Mbipia spp. and Pundamilia spp.) in the evolutionary history of these five species that would have lead to the evolution of novel trait combinations and new species.

Positive Darwinian Selection Drives the Evolution of the Morphology-Related Gene, EPCAM, in Particularly Species-Rich Lineages of African Cichlid Fishes

The study of genetic evolution within the context of adaptive radiations offers insights to genes and selection pressures that result in rapid morphological change. Cichlid fishes are very species-rich and variable in coloration, behavior, and morphology, and so provide a classical model system for studying the genetics of adaptive radiation. In this study, we researched the evolution of the epithelial cell adhesion molecule (EPCAM), a candidate gene for the adaptive evolution of morphology broadly, and skin development specifically, in fishes. We compared EPCAM gene sequences from a rapidly speciating African cichlid lineage (the haplochromines), a species-poor African lineage (Nile tilapia Oreochromis niloticus), and a very young adaptive radiation in the Neotropics (sympatric crater lake Midas cichlids, Amphilophus sp.). Our results, based on a hierarchy of evolutionary analyses of nucleotide substitution, demonstrate that there are different selection pressures on the EPCAM gene among the cichlid lineages. Several waves of positive natural selection were identified not only on the terminal branches, but also on ancestral branches. Interestingly, significant positive or directional selection was found in the haplochromine cichlids only but not the comparatively species-poor tilapia lineage. We hypothesize that the strong signal of selection in the ancestral African cichlid lineage coincided with the transition from riverine to lacustrine habitat. The two neotropical species for which we collected new sequence data were invariant in the EPCAM locus. Our results suggest that functional changes promoted by positive Darwinian selection are widespread in the EPCAM gene during African cichlid evolution.

Divergence along a steep ecological gradient in lake whitefish (Coregonussp.)

To understand mechanisms structuring diversity in young adaptive radiations, quantitative and unbiased information about genetic and phenotypic diversity is much needed. Here, we present the first in-depth investigation of whitefish diversity in a Swiss lake, with continuous spawning habitat sampling in both time and space. Our results show a clear cline like pattern in genetics and morphology of populations sampled along an ecological depth gradient in Lake Neuchâtel. Divergent natural selection appears to be involved in shaping this cline given that trait specific P(ST)-values are significantly higher than F(ST)-values when comparing populations caught at different depths. These differences also tend to increase with increasing differences in depth, indicating adaptive divergence along a depth gradient, which persists despite considerable gene flow between adjacent demes. It however remains unclear, whether the observed pattern is a result of currently stable selection-gene flow balance, incipient speciation, or reverse speciation due to anthropogenic habitat alteration causing two formerly divergent species to collapse into a single gene pool.

Patterns of genetic variation in the adaptive radiation of New World crossbills (Aves:Loxia)

Incipient species groups or young adaptive radiations such as crossbills (Aves: Loxia) present the opportunity to investigate directly the processes occurring during speciation. New World crossbills include white-winged crossbills (Loxia leucoptera), Hispaniolan crossbills (Loxia megaplaga), and red crossbills (Loxia curvirostra complex), the last of which is comprised of at least nine morphologically and vocally differentiated forms ('call types') where divergent natural selection for specialization on different conifer resources has been strongly implicated as driving diversification. Here we use amplified fragment length polymorphism (AFLP) markers to investigate patterns of genetic variation across populations, call types, and species of New World crossbills. Tree-based analyses using 440 AFLP loci reveal strongly supported clustering of the formally recognized species, but did not separate individuals from the eight call types in the red crossbill complex, consistent with recent divergence and ongoing gene flow. Analyses of genetic differentiation based on inferred allele frequency variation however, reveal subtle but significant levels of genetic differentiation among the different call types of the complex and indicate that between call-type differentiation is greater than that found among different geographic locations within call types. Interpreted in light of evidence of divergent natural selection and strong premating reproductive isolation, the observed genetic differentiation suggests restricted gene flow among sympatric call types consistent with the early stages of ecological speciation.

Ecological Character Displacement

Some morphological differences between closely related species living in the same environment have been enhanced by natural selection resulting from competition between the species or the negative effects of interbreeding. These evolutionary changes are known as ecological and reproductive character displacement, respectively. Ecological character displacement, the subject of this article, helps us to understand how complex communities are built up from simpler ones through ecological adjustments of the constituent species. It also may be involved in the late stages in speciation when formerly allopatric populations come together in sympatry. Examples are given from studies of birds in nature and sticklebacks in experiments. There are few cases of ecological character displacement in nature where the evidence is sufficiently strong to demonstrate evolution by natural selection and to rule out alternative explanations of the causes. These have been supplemented by experiments: there is scope and need for more. Key Concepts: Character displacement is a process of evolutionary divergence of coexisting species. Competition for resources, such as food, is reduced as a result of divergence. Natural selection causes the evolutionary change. Closely related species differ in morphology more in sympatry than in allopatry. Experiments attempt to recreate conditions that are conducive to character displacement in nature. Solitary species are released from competition and broaden their ecological niches. Character displacement helps to explain how complex communities of potential competitors develop from simple ones. Character displacement is one of several types of evolutionary adjustments made by coexisting species. Its signature should be seen most clearly in young adaptive radiations. The main question about character displacement is not whether it occurs but how important it is. Keywords: divergence; competition; food; natural selection; evolution; adaptive radiation