Cranial shape evolution in adaptive radiations of birds: comparative morphometrics of Darwin's finches and Hawaiian honeycreepers

Adaptive radiation is the rapid evolution of morphologically and ecologically diverse species from a single ancestor. The two classic examples of adaptive radiation are Darwin's finches and the Hawaiian honeycreepers, which evolved remarkable levels of adaptive cranial morphological variation. To gain new insights into the nature of their diversification, we performed comparative three-dimensional geometric morphometric analyses based on X-ray microcomputed tomography (µCT) scanning of dried cranial skeletons. We show that cranial shapes in both Hawaiian honeycreepers and Coerebinae (Darwin's finches and their close relatives) are much more diverse than in their respective outgroups, but Hawaiian honeycreepers as a group display the highest diversity and disparity of all other bird groups studied. We also report a significant contribution of allometry to skull shape variation, and distinct patterns of evolutionary change in skull morphology in the two lineages of songbirds that underwent adaptive radiation on oceanic islands. These findings help to better understand the nature of adaptive radiations in general and provide a foundation for future investigations on the developmental and molecular mechanisms underlying diversification of these morphologically distinguished groups of birds. This article is part of the themed issue ‘Evo-devo in the genomics era, and the origins of morphological diversity’.

Download Full-text

The consequences of craniofacial integration for the adaptive radiations of Darwin’s finches and Hawaiian honeycreepers

Nature Ecology & Evolution ◽

10.1038/s41559-019-1092-y ◽

2020 ◽

Vol 4 (2) ◽

pp. 270-278 ◽

Cited By ~ 6

Author(s):

Guillermo Navalón ◽

Jesús Marugán-Lobón ◽

Jen A. Bright ◽

Christopher R. Cooney ◽

Emily J. Rayfield

Keyword(s):

Darwin's Finches ◽

Hawaiian Honeycreepers ◽

Darwin’S Finches ◽

Adaptive Radiations

Download Full-text

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

Download Full-text

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.

Download Full-text

Host–pathogen coevolution, secondary sympatry and species diversification

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2009.0279 ◽

2010 ◽

Vol 365 (1543) ◽

pp. 1139-1147 ◽

Cited By ~ 70

Author(s):

Robert E. Ricklefs

Keyword(s):

Apparent Competition ◽

Allopatric Speciation ◽

Similar Reasoning ◽

Species Diversification ◽

Darwin's Finches ◽

Hawaiian Honeycreepers ◽

Darwin’S Finches ◽

Host Pathogen

The build-up of species locally within a region by allopatric speciation depends on geographically separated (allopatric) sister populations becoming reproductively incompatible followed by secondary sympatry. Among birds, this has happened frequently in remote archipelagos, spectacular cases including the Darwin's finches (Geospizinae) and Hawaiian honeycreepers (Drepanidinae), but similar examples are lacking in archipelagos nearer to continental landmasses. Of the required steps in the speciation cycle, achievement of secondary sympatry appears to be limiting in near archipelagos and, by extension, in continental regions. Here, I suggest that secondary sympatry might be prevented by apparent competition mediated through pathogens that are locally coevolved with one population of host and are pathogenic in sister populations. The absence of numerous pathogens in remote archipelagos might, therefore, allow sister populations to achieve secondary sympatry more readily and thereby accelerate diversification. By similar reasoning, species should accumulate relatively slowly within continental regions. In this essay, I explore the assumptions and some implications of this model for species diversification.

Download Full-text

The tale of the finch: adaptive radiation and behavioural flexibility

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2009.0291 ◽

2010 ◽

Vol 365 (1543) ◽

pp. 1099-1109 ◽

Cited By ~ 96

Author(s):

Sabine Tebbich ◽

Kim Sterelny ◽

Irmgard Teschke

Keyword(s):

Adaptive Radiation ◽

Darwin's Finches ◽

Genetic Accommodation ◽

Darwin’S Finches ◽

Morphological Adaptations ◽

Extra Factor ◽

Extraordinary Means ◽

Flexible Stem ◽

Innovative Techniques ◽

Current Behaviour

Darwin's finches are a classic example of adaptive radiation. The ecological diversity of the Galápagos in part explains that radiation, but the fact that other founder species did not radiate suggests that other factors are also important. One hypothesis attempting to identify the extra factor is the flexible stem hypothesis, connecting individual adaptability to species richness. According to this hypothesis, the ancestral finches were flexible and therefore able to adapt to the new and harsh environment they encountered by exploiting new food types and developing new foraging techniques. Phenotypic variation was initially mediated by learning, but genetic accommodation entrenched differences and supplemented them with morphological adaptations. This process subsequently led to diversification and speciation of the Darwin's finches. Their current behaviour is consistent with this hypothesis as these birds use unusual resources by extraordinary means. In this paper, we identify cognitive capacities on which flexibility and innovation depend. The flexible stem hypothesis predicts that we will find high levels of these capacities in all species of Darwin's finches (not just those using innovative techniques). Here, we test that prediction, and find that while most of our data are in line with the flexible stem hypothesis, some are in tension with it.

Download Full-text

Scaling and shear transformations capture beak shape variation in Darwin’s finches

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.0911575107 ◽

2010 ◽

Vol 107 (8) ◽

pp. 3356-3360 ◽

Cited By ~ 40

Author(s):

O. Campàs ◽

R. Mallarino ◽

A. Herrel ◽

A. Abzhanov ◽

M. P. Brenner

Keyword(s):

Shape Variation ◽

Darwin's Finches ◽

Beak Shape ◽

Darwin’S Finches

Download Full-text

Radula diversification promotes ecomorph divergence in an adaptive radiation of freshwater snails

10.1101/2020.01.17.910034 ◽

2020 ◽

Author(s):

Leon Hilgers ◽

Stefanie Hartmann ◽

Jobst Pfaender ◽

Nora Lentge-Maaß ◽

Thomas von Rintelen ◽

...

Keyword(s):

Adaptive Radiation ◽

Complex Traits ◽

Molecular Basis ◽

Molecular Mechanisms ◽

Freshwater Snail ◽

Freshwater Snails ◽

Trophic Specialization ◽

Adaptive Diversification ◽

Adaptive Radiations ◽

Lineage Divergence

AbstractAdaptive diversification of complex traits plays a pivotal role for the evolution of organismal diversity. However, the underlying molecular mechanisms remain largely elusive. In the freshwater snail genus Tylomelania, adaptive radiations were likely promoted by trophic specialization via diversification of their key foraging organ, the radula. To investigate the molecular basis of radula diversification and its contribution to lineage divergence, we use pooled tissue-specific transcriptomes of two sympatric Tylomelania sarasinorum ecomorphs. We show that divergence in both gene expression and coding sequences is stronger between radula transcriptomes compared to mantle and foot transcriptomes. These findings support the hypothesis that diversifying selection on the radula is driving speciation in Tylomelania radiations. We also identify several candidate genes for radula divergence. Putative homologs of some candidates (hh, arx, gbb) also contributed to trophic specialization in cichlids and Darwin’s finches, indicating that some molecular pathways may be especially prone to adaptive diversification.

Download Full-text

Molecular mechanisms underlying nuchal hump formation in dolphin cichlid, Cyrtocara moorii

Scientific Reports ◽

10.1038/s41598-019-56771-7 ◽

2019 ◽

Vol 9 (1) ◽

Cited By ~ 1

Author(s):

Laurène Alicia Lecaudey ◽

Christian Sturmbauer ◽

Pooja Singh ◽

Ehsan Pashay Ahi

Keyword(s):

Central America ◽

Adaptive Radiation ◽

Expression Profiling ◽

Molecular Mechanisms ◽

Soft Tissues ◽

Molecular Level ◽

Teleost Fishes ◽

East African ◽

Rapid Speciation ◽

Adaptive Radiations

AbstractEast African cichlid fishes represent a model to tackle adaptive changes and their connection to rapid speciation and ecological distinction. In comparison to bony craniofacial tissues, adaptive morphogenesis of soft tissues has been rarely addressed, particularly at the molecular level. The nuchal hump in cichlids fishes is one such soft-tissue and exaggerated trait that is hypothesized to play an innovative role in the adaptive radiation of cichlids fishes. It has also evolved in parallel across lakes in East Africa and Central America. Using gene expression profiling, we identified and validated a set of genes involved in nuchal hump formation in the Lake Malawi dolphin cichlid, Cyrtocara moorii. In particular, we found genes differentially expressed in the nuchal hump, which are involved in controlling cell proliferation (btg3, fosl1a and pdgfrb), cell growth (dlk1), craniofacial morphogenesis (dlx5a, mycn and tcf12), as well as regulators of growth-related signals (dpt, pappa and socs2). This is the first study to identify the set of genes associated with nuchal hump formation in cichlids. Given that the hump is a trait that evolved repeatedly in several African and American cichlid lineages, it would be interesting to see if the molecular pathways and genes triggering hump formation follow a common genetic track or if the trait evolved in parallel, with distinct mechanisms, in other cichlid adaptive radiations and even in other teleost fishes.

Download Full-text