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 .

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Genes controlling beak size and shape in Darwin's finches

AccessScience ◽

10.1036/1097-8542.yb170504 ◽

2017 ◽

Keyword(s):

Darwin's Finches ◽

Size And Shape ◽

Darwin’S Finches ◽

Beak Size

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Faculty Opinions recommendation of Gene flow, ancient polymorphism, and ecological adaptation shape the genomic landscape of divergence among Darwin's finches.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.727555631.793536812 ◽

2017 ◽

Author(s):

Thomas Mitchell-Olds ◽

Baosheng Wang ◽

Julius Mojica

Keyword(s):

Gene Flow ◽

Ecological Adaptation ◽

Darwin's Finches ◽

Darwin’S Finches ◽

Genomic Landscape

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Shallow genetic divergence and distinct phenotypic differences between two Andean hummingbirds: Speciation with gene flow?

The Auk ◽

10.1093/auk/ukz046 ◽

2019 ◽

Vol 136 (4) ◽

Cited By ~ 3

Author(s):

Catalina Palacios ◽

Silvana García-R ◽

Juan Luis Parra ◽

Andrés M Cuervo ◽

F Gary Stiles ◽

...

Keyword(s):

Gene Flow ◽

Genetic Differentiation ◽

Incomplete Lineage Sorting ◽

Lineage Sorting ◽

Phenotypic Differences ◽

Adaptive Mechanisms ◽

The Face ◽

Gloger’S Rule ◽

Divergence With Gene Flow ◽

Neutral Markers

Abstract Ecological speciation can proceed despite genetic interchange when selection counteracts the homogenizing effects of migration. We tested predictions of this divergence-with-gene-flow model in Coeligena helianthea and C. bonapartei, 2 parapatric Andean hummingbirds with marked plumage divergence. We sequenced putatively neutral markers (mitochondrial DNA [mtDNA] and nuclear ultraconserved elements [UCEs]) to examine genetic structure and gene flow, and a candidate gene (MC1R) to assess its role underlying divergence in coloration. We also tested the prediction of Gloger’s rule that darker forms occur in more humid environments, and examined morphological variation to assess adaptive mechanisms potentially promoting divergence. Genetic differentiation between species was low in both ND2 and UCEs. Coalescent estimates of migration were consistent with divergence with gene flow, but we cannot reject incomplete lineage sorting reflecting recent speciation as an explanation for patterns of genetic variation. MC1R variation was unrelated to phenotypic differences. Species did not differ in macroclimatic niches but were distinct in morphology. Although we reject adaptation to variation in macroclimatic conditions as a cause of divergence, speciation may have occurred in the face of gene flow driven by other ecological pressures or by sexual selection. Marked phenotypic divergence with no neutral genetic differentiation is remarkable for Neotropical birds, and makes C. helianthea and C. bonapartei an appropriate system in which to search for the genetic basis of species differences employing genomics.

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Divergence and gene flow among Darwin's finches: A genome-wide view of adaptive radiation driven by interspecies allele sharing

BioEssays ◽

10.1002/bies.201500047 ◽

2015 ◽

Vol 37 (9) ◽

pp. 968-974 ◽

Cited By ~ 13

Author(s):

Daniela H. Palmer ◽

Marcus R. Kronforst

Keyword(s):

Gene Flow ◽

Adaptive Radiation ◽

Allele Sharing ◽

Darwin's Finches ◽

Darwin’S Finches ◽

Genome Wide ◽

A Genome

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

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1813662115 ◽

2018 ◽

Vol 115 (46) ◽

pp. E10879-E10887 ◽

Cited By ~ 13

Author(s):

Peter R. Grant ◽

B. Rosemary Grant

Keyword(s):

Natural Habitat ◽

Good Choice ◽

Premating Isolation ◽

Sexual Imprinting ◽

Darwin's Finches ◽

Darwin’S Finches ◽

Adaptive Radiations ◽

Beak Size ◽

Species Specific

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.

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Mechanical stress, fracture risk and beak evolution in Darwin's ground finches ( Geospiza )

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2009.0280 ◽

2010 ◽

Vol 365 (1543) ◽

pp. 1093-1098 ◽

Cited By ~ 44

Author(s):

Joris Soons ◽

Anthony Herrel ◽

Annelies Genbrugge ◽

Peter Aerts ◽

Jeffrey Podos ◽

...

Keyword(s):

Common Ancestor ◽

High Stress ◽

Natural Populations ◽

Peak Stress ◽

Food Type ◽

Darwin's Finches ◽

Darwin’S Finches ◽

Competition For Food ◽

Selection For ◽

Beak Size

Darwin's finches have radiated from a common ancestor into 14 descendent species, each specializing on distinct food resources and evolving divergent beak forms. Beak morphology in the ground finches ( Geospiza ) has been shown to evolve via natural selection in response to variation in food type, food availability and interspecific competition for food. From a mechanical perspective, however, beak size and shape are only indirectly related to birds' abilities to crack seeds, and beak form is hypothesized to evolve mainly under selection for fracture avoidance. Here, we test the fracture-avoidance hypothesis using finite-element modelling. We find that across species, mechanical loading is similar and approaches reported values of bone strength, thus suggesting pervasive selection on fracture avoidance. Additionally, deep and wide beaks are better suited for dissipating stress than are more elongate beaks when scaled to common sizes and loadings. Our results illustrate that deep and wide beaks in ground finches enable reduction of areas with high stress and peak stress magnitudes, allowing birds to crack hard seeds while limiting the risk of beak failure. These results may explain strong selection on beak depth and width in natural populations of Darwin's finches.

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Gene flow, ancient polymorphism, and ecological adaptation shape the genomic landscape of divergence among Darwin's finches

Genome Research ◽

10.1101/gr.212522.116 ◽

2017 ◽

Vol 27 (6) ◽

pp. 1004-1015 ◽

Cited By ~ 57

Author(s):

Fan Han ◽

Sangeet Lamichhaney ◽

B. Rosemary Grant ◽

Peter R. Grant ◽

Leif Andersson ◽

...

Keyword(s):

Gene Flow ◽

Ecological Adaptation ◽

Darwin's Finches ◽

Darwin’S Finches ◽

Genomic Landscape

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THE EVOLUTIONARY HISTORY OF DARWIN'S FINCHES: SPECIATION, GENE FLOW, AND INTROGRESSION IN A FRAGMENTED LANDSCAPE

Evolution ◽

10.1111/evo.12484 ◽

2014 ◽

Vol 68 (10) ◽

pp. 2932-2944 ◽

Cited By ~ 43

Author(s):

Heather L. Farrington ◽

Lucinda P. Lawson ◽

Courtney M. Clark ◽

Kenneth Petren

Keyword(s):

Gene Flow ◽

Evolutionary History ◽

Fragmented Landscape ◽

Darwin's Finches ◽

Darwin’S Finches ◽

History Of

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Shallow evolutionary divergence between two Andean hummingbirds: Speciation with gene flow?

10.1101/249755 ◽

2018 ◽

Author(s):

Catalina Palacios ◽

Silvana García-R ◽

Juan Luis Parra ◽

Andrés M. Cuervo ◽

F. Gary Stiles ◽

...

Keyword(s):

Gene Flow ◽

Genetic Differentiation ◽

Genetic Basis ◽

Flow Model ◽

Evolutionary Divergence ◽

Phenotypic Differences ◽

Adaptive Mechanisms ◽

The Face ◽

Divergence With Gene Flow ◽

Neutral Markers

AbstractEcological speciation can proceed despite genetic interchange when selection counteracts homogeneizing effects of migration. We tested predictions of this divergence-with-gene-flow model in Coeligena helianthea and C. bonapartei, two parapatric Andean hummigbirds with marked plumage divergence. We sequenced neutral markers (mtDNA and nuclear ultra conserved elements) to examine genetic structure and gene flow, and a candidate gene (MC1R) to assess its role underlying divergence in coloration. We also tested the prediction of Glogers’ rule that darker forms occur in more humid environments, and compared ecomorphological variables to assess adaptive mechanisms potentially promoting divergence. Genetic differentiation between species was very low and coalescent estimates of migration were consistent with divergence with gene flow. MC1R variation was unrelated to phenotypic differences. Species did not differ in macroclimatic niches but were distinct in ecomorphology. Although we reject adaptation to variation in humidity as the cause of divergence, we hypothesize that speciation likely occurred in the face of gene flow, driven by other ecological pressures or by sexual selection. Marked phenotypic divergence with no neutral genetic differentiation is remarkable for Neotropical birds, and makes C. helianthea and C. bonapartei an appropriate system in which to search for the genetic basis of species differences employing genomics.

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