In other species: Great Tit , black-bellied seedcracker

Categories: Craniofacial phene

Links to possible relevant human trait(s) and/or gene(s) in OMIM: 600698 (gene)

Mendelian trait/disorder: no

Mode of inheritance: Multifactorial

Disease-related: no

Key variant known: no

Key variant is published: no

Cross-species summary: Bill size

Species-specific description: Darwin (1859) recognised the importance of an evolutionary phenomenon he called divergence of character. As explained by Lamichhaney et al. (2016), an excellent example of divergence of character (now called ecological character displacement) is provided by competition between "The medium ground finch (Geospiza fortis) and large ground finch (G. magnirostris) on the small island of Daphne Major" during a severe drought in 2004-2005. Exploiting the enormous potential of whole-genome sequence data, Lamichhaney et al. (2016) "discovered a genomic region containing the HMGA2 gene that varies systematically among Darwin’s finch species with different beak sizes. Two haplotypes [containing this gene] . . . were involved in the character displacement event: Genotypes associated with large beak size were at a strong selective disadvantage in medium ground finches (selection coefficient s = 0.59). Thus, a major locus has apparently facilitated a rapid ecological diversification in the adaptive radiation of Darwin’s finches."

History: Variation in beak shape and size between species of finches on different islands of the Galapagos archipelago has become one of the textbook examples of evolution. This variation was first noted by Charles Darwin, following his visit to the archipelago in 1835 during the round-the-world voyage of HMS Beagle. Darwin did not mention the variation in the diary he wrote at the time of the visit, but did mention it in his published journal of the voyage (Darwin, 1839): "It is very remarkable that a nearly perfect gradation of structure in this one group can be traced in the form of the beak, from one exceeding in dimensions that of the largest gros-beak, to another differing but little from that of a warbler. [pp. 461-462] . . . I have stated, that in the thirteen species of ground-finches, a nearly perfect gradation may be traced, from a beak extraordinarily thick, to one so fine, that it may be compared to that of a warbler. I very much suspect, that certain members of the series are confined to different islands; therefore, if the collection had been made on any one island, it would not have presented so perfect a gradation. It is clear, that if several islands have each their peculiar species of the same genera, when these are placed together, they will have a wide range of character. But there is not space in this work, to enter on this curious subject. [p. 475]" By the time of the second edition of this journal, published in 1845, Darwin had more to say on the variation in beak shape and size: "The most curious fact is the perfect gradation in the size of the beaks in the different species of Geospiza, from one as large as that of a hawfinch to that of a chaffinch, and (if Mr. Gould is right in including his sub-group, Certhidea, in the main group), even to that of a warbler. The largest beak in the genus Geospiza is shown in Fig. 1, and the smallest in Fig. 3; but instead of there being only one intermediate species, with a beak of the size shown in Fig. 2, there are no less than six species with insensibly graduated beaks. The beak of the sub-group Certhidea, is shown in Fig. 4. The beak of Cactornis is somewhat like that of a starling; and that of the fourth sub-group, Camarhynchus, is slightly parrot-shaped. Seeing this gradation and diversity of structure in one small, intimately related group of birds, one might really fancy that from an original paucity of birds in this archipelago, one species had been taken and modified for different ends. [pp. 379-380]". The reference to figures relates to a plate in the 1845 journal, illustrating the contrasting beak shapes and sizes of four Galapagos finches. Interestingly, Darwin makes no mention of Galapagos finches in any edition of Origin of Species, because (despite his earlier surmises above), he never had sufficient information on the available specimens to enable him to draw firm conclusions about evolution. Ironically, it was not until many decades after Darwin's death that sufficient information had been gathered on Galapagos finches (see, e.g., Lack, 1947) to enable them to become a classic textbook example of evolution.

Mapping: Lamichhaney et al. (2016) sequenced 10 each of six Galapagos finch species: small, medium and large ground finches and small, medium and large tree finches. Comparison of large vs small, large vs medium, and medium vs small (pooled across ground and tree species, and separately in each) identified a 525kb region that showed the strongest differentiation in all contrasts. This region contains four genes, the most likely candidate being HMGA2, which is associated with size in mice, humans, horses (see OMIA 001968-9796) and dogs (see OMIA 001968-9615).

Molecular basis: Lamichhaney et al. (2016) genotyped a diagnostic SNP for the two HMGA2 haplotypes in 133 medium ground finches and discovered that this locus showed a highly significant additive effect on beak size, accounting for "as much as 27% of the phenotypic variance [in beak size] in this population". Comparison of medium ground finches from the island of Daphne Major that survived or died in the 2004-2005 drought led Lamichhaney et al. (2016) to conclude that HMGA2 caused about 30% of the shift in beak size and "the relationship between HMGA2 and fitness was mediated entirely by the effect of this locus on beak size or associated craniofacial bones or muscles". (with thanks to Leif Andersson for feedback on an earlier version of the text on this page) Enbody et al. (2023): "Using whole-genome data of 3955 of Darwin’s finches on the Galápagos Island of Daphne Major, [the authors] identified six loci of large effect that explain 45% of the variation in the highly heritable beak size of Geospiza fortis, a key ecological trait."

Associated gene: