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

Abstract

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’.

The association between morphological and ecological characters across a global passerine radiation

“…A key message from the results of this analysis is that whereas morphology is generally a good predictor of broad ecological differences among species (Figure ), ecological variables have limited ability to predict morphological variation (Table ; Table S15; see also Felice et al, ; Miles & Ricklefs, ; Navalón et al, ). These patterns are seemingly in contrast to the tight and reciprocal associations between ecology and morphology that have been shown among adaptive radiations, such as Darwin's finches and Hawaiian honeycreepers (Tokita, Yano, James, & Abzhanov, ). The coarse nature of the ecological character states may provide significant explanation for the lower explanatory power of the models using these variables to predict morphological variation (Felice et al, ).…”

Evolution of cranial shape in a continental‐scale evolutionary radiation of Australian lizards

“…Additionally, patterns like these have been observed in certain species of birds (Tokita et al. ), mammals (Goswami et al. ), and fish (Clabaut et al.…”

Perspectives on the history of evo-devo and the contemporary research landscape in the genomics era

“…As in the past, phylogeny is inferred from comparative studies of living organisms but these comparisons can now be made at all three levels: comparative anatomy, comparative development and comparative genomics. The article by Arkhat Abzhanov and co-workers in this issue [45] on shape of the cranium in various species of birds illustrates a modern approach to comparative anatomy, while the article by Tucker [46] on the evolution of the mammalian middle ear illustrates how comparative development is currently being studied.…”

“…Major morphological transitions and innovations are considered first with articles on the origins of animal multicellularity from a classical perspective by Cavalier-Smith [52] and illustrating the impact of genomics by Babonis & Martindale [20] and an article on the evolution of land plants by Harrison [53]; the major transition that created the unique mammalian middle ear is discussed by Tucker [46]. The next section focuses on diversification and modifications of morphology as exemplified by tetrapod limbs by Saxena et al [54], flowers by Pam Soltis and co-workers [55], cranial shape in birds by Abzhanov and co-workers [45] and wing coloration patterns in butterflies by Jiggins et al [56]. The last section considers the relatively recent evolution of genetically determined morphological variation within a single species owing to either natural selection, using as examples, cavefish (article by Krishnan & Rohner [57]) and stickleback (article by Piechel & Marques [58]) or artificial selection, using dogs as an example (article by Elaine Ostrander and co-workers [59]) and ends with the article on developmental plasticity by Xu & Zhang [49].…”

“…There are an increasing number of genome-wide analyses aiming to identify differences in gene expression in developing organs of different organisms, including, for example, comparisons between mouse, chimpanzee and human (reviewed in [66]). Interpretation of positional information may often involve fine-tuning morphogenesis and the spatial coordination of various cell activities such as movement, adhesiveness and proliferation to produce for example the specific shapes of the bird cranium [45] or the bones in vertebrate limb digits [54] or the scale structure in Heliconius butterflies [56]. At first sight, the dissection of how such complex processes are fine-tuned seems very daunting but recent work has shown that morphogenesis can proceed-apparently spontaneously-given the right conditions.…”