Habitat selection and ecological speciation in Galápagos warbler finches (Certhidea olivacea and Certhidea fusca)

We investigated phylogeographic divergence among populations of Galápagos warble finches. Their broad distribution, lack of phenotypic differentiation and low levels of genetic divergence make warbler finches an appropriate model to study speciation in allopatry. A positive relationship between genetic and geographical distance is expected for island taxa. Warbler finches actually showed a negative isolation by distance relationship, causing us to reject the hypothesis of distance-limited dispersal. An alternative hypothesis, that dispersal is limited by habitat similarity, was supported. We found a positive correlation between genetic distances and differences in maximum elevation among islands, which is an indicator of ecological similarity. MtDNA sequence variation revealed monophyletic support for two distinct species. Certhidea olivacea have recently dispersed among larger central islands, while some Certhidea fusca have recently dispersed to small islands at opposite ends of the archipelago. We conclude that females have chosen to breed on islands with habitats similar to their natal environment. Habitat selection is implicated as an important component of speciation of warbler finches, which is the earliest known divergence of the adaptive radiation of Darwin's finches. These results suggest that small populations can harbour cryptic but biologically meaningful variation that may affect longer term evolutionary processes.     

Lack of premating isolation at the base of a phylogenetic tree

Darwin's finches in the Galápagos archipelago are an unusual example of adaptive radiation in that the basal split separates two lineages of warbler finches (Certhidea olivacea and Certhidea fusca) believed until recently to be only one species. The large genetic difference between them contrasts with their similarity in plumage, size, shape, and courtship behavior. They differ in song, which is a key factor in premating isolation of other sympatric Darwin's finches. We conducted playback experiments to see whether members of the population of C. olivacea on Santa Cruz Island would respond to songs of C. fusca from two islands, Genovesa and Pinta, and songs of C. olivacea from another island (Isabela). Another set of experiments was performed, using the same playback tapes, with C. fusca on Genovesa. Some members of both populations responded to all playbacks; therefore, the hypothesis of complete premating isolation on the basis of song is rejected. Discrimination between songs of the two lineages was inconsistent. We conclude that premating barriers to interbreeding among the tested populations have not arisen in the 1.5-2.0 m.yr. of their geographical isolation on different islands. This contrasts with strong premating barriers between more recently derived sympatric species. Early learning of song associated with morphology is later used in mate recognition. This explains why sympatric species that are vocally and morphologically distinct yet genetically less differentiated than Certhidea do not interbreed, whereas the Certhidea lineages that are genetically well differentiated but vocally and morphologically similar have no apparent premating barrier. We discuss this unusual situation in terms of the forces that have produced similarities and differences in song, morphology, and ecology and their relevance to phylogenetic and biological species concepts. Neither principles nor details are unique to Darwin's finches, and we conclude by pointing out strong parallels with some continental birds.     

Divergence with gene flow as facilitated by ecological differences: within-island variation in Darwin's finches

Divergence and speciation can sometimes proceed in the face of, and even be enhanced by, ongoing gene flow. We here study divergence with gene flow in Darwin''s finches, focusing on the role of ecological/adaptive differences in maintaining/promoting divergence and reproductive isolation. To this end, we survey allelic variation at 10 microsatellite loci for 989 medium ground finches (Geospiza fortis) on Santa Cruz Island, Galápagos. We find only small genetic differences among G. fortis from different sites. We instead find noteworthy genetic differences associated with beak. Moreover, G. fortis at the site with the greatest divergence in beak size also showed the greatest divergence at neutral markers; i.e. the lowest gene flow. Finally, morphological and genetic differentiation between the G. fortis beak-size morphs was intermediate to that between G. fortis and its smaller (Geospiza fuliginosa) and larger (Geospiza magnirostris) congeners. We conclude that ecological differences associated with beak size (i.e. foraging) influence patterns of gene flow within G. fortis on a single island, providing additional support for ecological speciation in the face of gene flow. Patterns of genetic similarity within and between species also suggest that interspecific hybridization might contribute to the formation of beak-size morphs within G. fortis.     

Reproductive isolation of sympatric morphs in a population of Darwin's finches

Recent research on speciation has identified a central role for ecological divergence, which can initiate speciation when (i) subsets of a species or population evolve to specialize on different ecological resources and (ii) the resulting phenotypic modes become reproductively isolated. Empirical evidence for these two processes working in conjunction, particularly during the early stages of divergence, has been limited. We recently described a population of the medium ground finch, Geospiza fortis, that features large and small beak morphs with relatively few intermediates. As in other Darwin's finches of the Galápagos Islands, these morphs presumably diverged in response to variation in local food availability and inter- or intraspecific competition. We here demonstrate that the two morphs show strong positive assortative pairing, a pattern that holds over three breeding seasons and during both dry and wet conditions. We also document restrictions on gene flow between the morphs, as revealed by genetic variation at 10 microsatellite loci. Our results provide strong support for the central role of ecology during the early stages of adaptive radiation.     

Non-random fitness variation in two populations of Darwin's finches

Darwinian fitness of an individual is measured by the number of recruits it contributes to the next generation. We studied variation in fitness among members of three cohorts of two species of Darwin's finches living on the Galipagos island of Daphne Major: the medium ground finch (Geospiza fortis) and cactus finch (Geospiza scandens). Individuals of both species live for up to 16 years. Variation in fitness was neither random nor heritable. Non-randomness arises as a result of a few individuals living for an exceptionally long time and breeding many times. For each cohort, the number of recruits per breeder is strongly predicted by the number of fledglings per breeder. In turn, the number of fledglings is strongly predicted by longevity of the breeder. These results suggest that the most important determinant of fitness is the ability of an individual to survive to breed in many years. Morphological traits affect this ability. Although morphological traits are heritable they do not change unidirectionally because they are selected in opposite directions, and in different combinations, under fluctuating environmental conditions. Non-random fitness variation in fluctuating populations implies much smaller genetically effective sizes than breeding population sizes.     

A phylogeny of Darwin's finches based on microsatellite DNA length variation

Allele length variation at 16 microsatellite loci was used to estimate the phylogeny of 13 out of the 14 species of Darwin''s finches. The resulting topology was similar to previous phylogenies based on morphological and allozyme variation. An unexpected result was that genetic divergence among Galápagos Island populations of the warbler finch (Certhidea olivacea) predates the radiation of all other Darwin''s finches. This deep split is surprising in view of the relatively weak morphological differentiation among Certhidea populations and supports the hypothesis that the ancestor of all Darwin''s finches was phenotypically similar to Certhidea. The results also resolve a biogeographical problem: the Cocos Island finch evolved after the Galápagos finch radiation was under way, supporting the hypothesis that this distant island was colonized from the Galápagos Islands. Monophyletic relationships are supported for both major groups, the ground finches (Geospiza) and the tree finches (Camarhynchus and Cactospiza), although the vegetarian finch (Platyspiza crassirostris) appears to have diverged prior to the separation of ground and tree finches. These results demonstrate the use of microsatellites for reconstructing phylogenies of closely related species and interpreting their evolutionary and biogeographic histories.     

Multilocus genotypes from Charles Darwin's finches: biodiversity lost since the voyage of the Beagle

Genetic analysis of museum specimens offers a direct window into a past that can predate the loss of extinct forms. We genotyped 18 Galápagos finches collected by Charles Darwin and companions during the voyage of the Beagle in 1835, and 22 specimens collected in 1901. Our goals were to determine if significant genetic diversity has been lost since the Beagle voyage and to determine the genetic source of specimens for which the collection locale was not recorded. Using ‘ancient’ DNA techniques, we quantified variation at 14 autosomal microsatellite loci. Assignment tests showed several museum specimens genetically matched recently field-sampled birds from their island of origin. Some were misclassified or were difficult to classify. Darwin''s exceptionally large ground finches (Geospiza magnirostris) from Floreana and San Cristóbal were genetically distinct from several other currently existing populations. Sharp-beaked ground finches (Geospiza difficilis) from Floreana and Isabela were also genetically distinct. These four populations are currently extinct, yet they were more genetically distinct from congeners than many other species of Darwin''s finches are from each other. We conclude that a significant amount of the finch biodiversity observed and collected by Darwin has been lost since the voyage of the Beagle.     

A phylogenetic reanalysis of allozyme variation among populations of Galapagos finches

We reanalysed Yang & Pattern's allozyme data, published in Auk in 1981, of Darwin's finches with a variety of distance and cladistic methods to estimate the phylogeny of the group. Different methods yielded different results, nevertheless there was widespread agreement among the distance methods on several groupings. First, the two species of Camarhynchus grouped near one another, but not always as a monophyletic group. Second, Cactospiza pallida and Platyspiza crassirostris formed a monophyletic group. Finally, all the methods (including parsimony) supported the monophyly of the ground finches. The three distance methods also found close relationships generally between each of two populations of Geospiza scandens, G. difficilis and G. conirostris. There is evidence for inconstancy of evolutionary rates among species. Results from distance methods allowing for rate variation among lineages suggest three conclusions which differ from Yang and Patton's findings. First, the monophyletic ground finches arose from the paraphyletic tree finches. Yang and Patton found that the ground finches and tree finches were sister monophyletic taxa. Second, Geospiza scandens appears to be a recently derived species, and not the most basal ground finch. Third, G. fuliginosa is not a recently derived species of ground finch, but was derived from an older split from the remaining ground finches. Most of these conclusions should be considered tentative both because the parsimony trees disagreed sharply with the distance trees and because no clades were strongly supported by the results of bootstrapping and statistical tests of alternative hypotheses. Absence of strong support for clades was probably due to insufficient data. Future phylogenetic studies, preferably using DNA sequence data from several unlinked loci, should sample several populations of each species, and should attempt to assess the importance of hybridization in species phylogeny.     

Inbreeding and interbreeding in Darwin's finches

Studies of inbreeding and interspecific hybridization are generally pursued separately with different metrics. There is a need to integrate them because they have the common goal of seeking an understanding of the genetic and ecological basis of fitness variation in populations. We use mean expected heterozygosity as an axis of variation on which to compare the fitness of inbreeding and hybridizing Darwin's finches (Geospiza scandens and G. fortis) relative to the fitness of matched outbred controls. We find that relative fitness of inbred finches is less than one in the 1991 cohorts of both species. Inbreeding depression is stronger in the species (G. scandens) with the lower genetically effective population size. Relative fitness of hybrids (backcrosses) in the same cohort of G. scandens is greater than one. Evidence of heterosis in G. fortis is mixed. Thus the two interbreeding species displayed somewhat different fitness patterns under the same set of environmental conditions. Hybridization may enhance fitness to different degrees by counteracting the effects of inbreeding depression, by other additive and nonadditive genetic effects, and by producing phenotypes well suited to exploit particular ecological conditions.     

Panmixia supports divergence with gene flow in Darwin's small ground finch, Geospiza fuliginosa, on Santa Cruz, Galápagos Islands

The divergence‐with‐gene‐flow model of speciation has a strong theoretical basis with a growing number of plausible examples in nature, but remains hotly debated. Darwin’s finches of the Galápagos Archipelago have played an important role in our understanding of speciation processes. Recent studies suggest that this group may also provide insights into speciation via divergence with gene flow. On the island of Santa Cruz, recent studies found evidence for adaptive divergence in Darwin’s small ground finch, Geospiza fuliginosa, between ecologically contrasting arid and humid zones. Despite the short geographical distance between these zones, strong disruptive selection during low rainfall periods is expected to generate and maintain adaptive divergence. Conversely, during high rainfall periods, when disruptive selection is predicted to be weakened, population divergence in adaptive traits is expected to break down. Because periods of low and high rainfall irregularly alternate, the geographical pattern of adaptive divergence can be assumed to break down and, importantly, regenerate in situ. Here, we use microsatellite allele frequency data to assess the genetic population structure of G. fuliginosa on Santa Cruz. We sample 21 sites and four ecological zones across the island. We reject hypotheses of population substructure linked to ecological and geographical differences among sites in favour of a single panmictic population. Panmixia implies high levels of gene flow within Santa Cruz, which favours selection over genetic drift as a valid process generating phenotypic divergence in G. fuliginosa on Santa Cruz. We discuss how our findings may support classic adaptation, phenotypic plasticity, matching habitat choice or any combination of these three processes.     

Fission and fusion of Darwin's finches populations

This study addresses the causes and evolutionary consequences of introgressive hybridization in the sympatric species of Darwin's ground finches (Geospiza) on the small island of Daphne Major in the Galápagos archipelago. Hybridization occurs rarely (less than 2% of breeding pairs) but persistently across years, usually as a result of imprinting on the song of another species. Hybrids survive well under some ecological conditions, but not others. Hybrids mate according to song type. The resulting introgression increases phenotypic and genetic variation in the backcrossed populations. Effects of introgression on beak shape are determined by the underlying developmental genetic pathways. Introgressive hybridization has been widespread throughout the archipelago in the recent past, and may have been a persistent feature throughout the early history of the radiation, episodically affecting both the speed and direction of evolution. We discuss how fission through selection and fusion through introgression in contemporary Darwin's finch populations may be a reflection of processes occurring in other young radiations. We propose that introgression has the largest effect on the evolution of interbreeding species after they have diverged in morphology, but before the point is reached when genetic incompatibilities incur a severe fitness cost.     

Hybridization in the recent past

The question we address in this article is how hybridization in the recent past can be detected in recently evolved species. Such species may not have evolved genetic incompatibilities and may hybridize with little or no fitness loss. Hybridization can be recognized by relatively small genetic differences between sympatric populations because sympatric populations have the opportunity to interbreed whereas allopatric populations do not. Using microsatellite DNA data from Darwin's finches in the Galapagos archipelago, we compare sympatric and allopatric genetic distances in pairs of Geospiza and Camarhynchus species. In agreement with the hybridization hypothesis, we found a statistically strong tendency for a species to be more similar genetically to a sympatric relative than to allopatric populations of that relative. Hybridization has been studied directly on two islands, but it is evidently more widespread in the archipelago. We argue that introgressive hybridization may have been a persistent feature of the adaptive radiation through most of its history, facilitating evolutionary diversification and occasionally affecting both the speed and direction of evolution.     

Do different rates of gene flow underlie variation in phenotypic and phenological clines in a montane grasshopper community?

Species responses to environmental change are likely to depend on existing genetic and phenotypic variation, as well as evolutionary potential. A key challenge is to determine whether gene flow might facilitate or impede genomic divergence among populations responding to environmental change, and if emergent phenotypic variation is dependent on gene flow rates. A general expectation is that patterns of genetic differentiation in a set of codistributed species reflect differences in dispersal ability. In less dispersive species, we predict greater genetic divergence and reduced gene flow. This could lead to covariation in life‐history traits due to local adaptation, although plasticity or drift could mirror these patterns. We compare genome‐wide patterns of genetic structure in four phenotypically variable grasshopper species along a steep elevation gradient near Boulder, Colorado, and test the hypothesis that genomic differentiation is greater in short‐winged grasshopper species, and statistically associated with variation in growth, reproductive, and physiological traits along this gradient. In addition, we estimate rates of gene flow under competing demographic models, as well as potential gene flow through surveys of phenological overlap among populations within a species. All species exhibit genetic structure along the elevation gradient and limited gene flow. The most pronounced genetic divergence appears in short‐winged (less dispersive) species, which also exhibit less phenological overlap among populations. A high‐elevation population of the most widespread species, Melanoplus sanguinipes, appears to be a sink population derived from low elevation populations. While dispersal ability has a clear connection to the genetic structure in different species, genetic distance does not predict growth, reproductive, or physiological trait variation in any species, requiring further investigation to clearly link phenotypic divergence to local adaptation.     

Darwin's finches: a model of landscape effects on metacommunity dynamics in the Galápagos Archipelago

Darwin's finches represent a dynamic radiation of birds within the Galápagos Archipelago. Unlike classic island radiations dominated by island endemics and intuitive ‘conveyer belt’ colonization with little subsequent dispersal, species of Darwin's finches have populations distributed across many islands and each island contains complex metacommunities of closely related birds. Understanding the role of metacommunity and structured population dynamics in speciation within this heterogeneous island system would provide insights into the roles of fragmentation and dispersal in evolution. In this study, a large multi‐species dataset and a comparative ground finch dataset (two co‐distributed lineages) were used to show how landscape features influence patterns of gene flow across the archipelago. Factors expected to regulate migration including distance and movement from large, central islands to small, peripheral islands were rejected in the multi‐species dataset. Instead, the harsh northeast islands contributed individuals to the larger central islands. Successful immigration relies on three factors: arriving, surviving and reproducing, thus the dispersal towards the central islands may be either be due to more migrants orienting towards these land masses due to their large size and high elevation, or may reflect a higher likelihood of survival and successful reproduction due to the larger diversity of habitats and more environmentally stable ecosystems that these islands possess. Further, the overall directionality of migration was south‐southwest against the dominant winds and currents. In comparing dispersal between the common cactus finch and medium ground finch, both species had similar migration rates but the cactus finch had approximately half the numbers of migrants due to lower effective populations sizes. Significant population structure in the cactus finch indicates potential for further speciation, while the medium ground finch maintains cohesive gene flow across islands. These patterns shed light on the macroevolutionary patterns that drive diversification and speciation within a radiation of highly‐volant taxa.     

Low genetic differentiation among reed warbler Acrocephalus scirpaceus populations across Europe

Migratory birds generally have higher dispersal propensity than resident species and are thus expected to show less genetic differentiation. On the other hand, specific migration patterns may promote genetic structure, such as in situations where migratory divides impede random mixing of individuals. Here we investigated population genetic structure and gene flow patterns in a polytypic passerine, the reed warbler Acrocephalus scirpaceus which shows a migratory divide in central Europe. Using ten polymorphic microsatellite loci and extensive sampling we found low but significant overall genetic differentiation (F_ST=0.013, G’_ST=0.078, D=0.063). Hierarchical F‐statistics and barrier analyses showed low but significant genetic differentiation of Iberian populations, and also slight genetic differences across the migratory divide and between subspecies (A. s. scirpaceus and A. s. fuscus). Three individual‐based Bayesian methods, however, inferred a single genetic unit. Our study thus found low levels of genetic differentiation among reed warbler populations but this genetic differentiation was not pronounced enough to detect a clear population structure using the microsatellite data and no prior information on geographic location of the sampled individuals. This result indicates high levels of gene flow and suggests a possibly recent divergence of European populations after a rapid range expansion. Further studies are necessary to assess divergence times and to reveal the evolutionary history of the reed warbler populations.     

Microevolutionary patterns and processes of the Native Hawaiian colonizing fern Odontosoria chinensis (Lindsaeaceae)

Abstract.— The vascular‐plant flora of the Hawaiian Islands is characterized by one of the highest rates of species endemism in the world. Among flowering plants, approximately 89% of species are endemic, and among pteridophytes, about 76% are endemic. At the single‐island level, however, rates of species endemism vary dramatically between these two groups with 80% of angiosperms and only 6% of pteridophytes being single‐island endemics. Thus, in many groups of Hawaiian angiosperms, it is possible to link studies of phylogeny, evolution, and biogeographic history at the interspecific and interisland levels. In contrast, the low level of single‐island species endemism among Hawaiian pteridophytes makes similar interspecific and interisland studies nearly impossible. Higher levels of interisland gene flow may account for the different levels of single‐island endemism in Hawaiian pteridophytes relative to angiosperms. The primary question we addressed in the present study was: Can we infer microevolutionary patterns and processes among populations within widespread species of Hawaiian pteridophytes wherein gene flow is probably common? To address this broad question, we conducted a population genetic study of the native Hawaiian colonizing species Odontosoria chinensis. Data from allozyme analyses allowed us to infer: (1) significant genetic differentiation among populations from different islands; (2) historical patterns of dispersal between particular pairs of islands; (3) archipelago‐level patterns of dispersal and colonization; (4) founder effects among populations on the youngest island of Hawaii; and, (5) that this species primarily reproduces via outcrossing, but may possess a mixed‐mating system.     

Genetic and morphological divergence at different spatiotemporal scales in the grasshopper Mioscirtus wagneri (Orthoptera: Acrididae)

The study of the association between morphological and genetic divergence can provide important information on the factors determining population differentiation and gene flow at different spatiotemporal scales. In this study we analyze the congruence between morphological and genetic divergence in the Iberian populations of Mioscirtus wagneri, a specialized grasshopper exclusively inhabiting highly fragmented hypersaline low grounds. We have found strong morphological variation among the studied localities and among mtDNA- and microsatellite-based genetic clusters. However, we have detected some cases of morphological convergence between highly differentiated populations. By contrast, certain genetically homogeneous populations at both mtDNA and microsatellite markers showed significant morphological differentiation which may be explained by phenotypic plasticity or divergent selection pressures acting at different spatiotemporal scales. Mantel tests also revealed that morphological divergence was associated with microsatellite- but not with mtDNA-based genetic distances. Overall, this study suggests that morphological traits can provide additional information on the underlying population genetic structure when only data on scarcely variable mtDNA markers is available. Thus, morphology can retain useful information on genetic structure and has the benefit over molecular methods of being inexpensive, offering a preliminary/complementary useful criterion for the establishment of management units necessary to guide conservation policies.     

The microevolution of the Galápagos marine iguana Amblyrhynchus cristatus assessed by nuclear and mitochondrial genetic analyses

Marine iguanas may have inhabited the Galápagos archipelago and its former, now sunken islands for more than 10 million years (Myr). It is therefore surprising that morphological and immunological data indicate little evolutionary divergence within the genus. We utilized mitochondrial DNA (mtDNA) sequence analyses and nuclear DNA fingerprinting to re-evaluate the level and pattern of genetic differentiation among 22 marine iguana populations from throughout the archipelago. Both genetic marker systems detect a low level of within-genus divergence, but they show contrasting levels of geographical subdivision among the populations. The mitochondrial gene pools of populations from different regions of the archipelago are isolated, and the mtDNA pattern appears to follow the sequence in which the islands were colonized by marine iguanas. Conversely, the nuclear DNA study indicates substantial interpopulational gene exchange, and the geographical distribution of the nuclear markers seems to be determined by isolation by distance among the populations. The natural history of marine iguanas suggests that the contrasting nuclear and mitochondrial DNA patterns result from an asymmetric migration behaviour of the two sexes, with higher (active and passive) interisland dispersal for males than females. Separate genetic analyses for the sexes appear to support this hypophesis. Based on these findings, a scenario is proposed that explains the marine iguanas' low genetic divergence, notwithstanding their long evolutionary history in the Galápagos archipelago.     

Naris and beak malformation caused by the parasitic fly, Philornis downsi (Diptera: Muscidae), in Darwin's small ground finch, Geospiza fuliginosa (Passeriformes: Emberizidae)

Parasites induce phenotypic modifications in their hosts, which can compromise host fitness. For example, the parasitic fly Philornis downsi , which was recently introduced to the Galápagos Islands, causes severe naris and beak malformation in Darwin's finches. The fly larvae feed on tissues from the nares of developing finch nestlings, thereby altering the size and shape of the nares and beak. Although the parasitism is age-specific (adult finches are not parasitized), naris and beak malformations persist into adulthood as parasite-induced malformations. We systematically examined adult populations of Darwin's small ground finch, Geospiza fuliginosa , on the islands of Santa Cruz for P. downsi -induced malformation. We found that malformed birds had significantly longer nares, and shorter, shallower beaks, than birds considered to be normal (i.e. with no nares or beak malformation). In addition, normal birds showed an isometry between naris length and beak dimensions (beak length feather and beak depth), which was not found in malformed birds. These differences suggest that beak morphology was influenced by P. downsi parasitism. Interestingly, we did not find any evidence of developmental impairment (smaller body size) or reduced foraging efficiency (lower body condition) between normal and malformed birds. Our findings of P. downsi -induced malformation raise new questions about the evolutionary trajectory and conservation status for this group of birds.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 577–585.