How did Darwin explain the evolution of the different species of Galapagos finches?

Darwin's finches, inhabiting the Galápagos archipelago and Cocos island, constitute an iconic model for studies of speciation and adaptive evolution. A team of scientists from Uppsala University and Princeton University has now shed light on the evolutionary history of these birds and identified a gene that explains variation in beak shape within and among species. The study is published today in Nature, on the day before the 206th anniversary of the birth of Charles Darwin.

Darwin's finches are a classical example of an adaptive radiation. Their common ancestor arrived on the Galapagos about two million years ago. During the time that has passed the Darwin's finches have evolved into 15 recognized species differing in body size, beak shape, song and feeding behaviour. Changes in the size and form of the beak have enabled different species to utilize different food resources such as insects, seeds, nectar from cactus flowers as well as blood from iguanas, all driven by Darwinian selection.

"We have now sequenced 120 birds including all known species of Darwin's finches, as well as two closely related species in order to study their evolutionary history," explains Sangeet Lamichhaney PhD student and shared first author on the paper. Multiple individuals of each species were analyzed and for some species birds from up to six different islands were sampled to study variation within and between islands.

One important insight was that gene flow between species has played a prominent role throughout the evolutionary history of the Darwin's finches. The scientists could even trace clear signs of hybridization between a warbler finch and the common ancestor of tree and ground finches that must have occurred about a million year ago.

"During our field work on the Galapagos we have observed many examples of hybridization between species of Darwin's finches but the long-term evolutionary effects of these hybridizations have been unknown," say Peter and Rosemary Grant, Princeton University, who know more about the biology of the Darwin's finches than anyone else in the world after carrying out field work on the Galapagos during a 40 year period.

"Now we can safely conclude that interspecies hybridization has played a critical role in the evolution of the finches, and has contributed to maintaining their genetic diversity," says Peter Grant.

The most striking phenotypic diversity among the Darwin's finches is the variation in the size and shape of the beaks. Charles Darwin was struck by this biological diversity, and compared it with the variety he was accustomed to among European birds such as the hawfinch, the chaffinch and warblers, as documented in his book "The Voyage of The Beagle." The team investigated the genetic basis for variation in beak shape by comparing two species with blunt beaks and two species with pointed beaks. Fifteen regions of the genome stood out as being very different in this contrast, and as many as six of these contained genes that previously have been associated with craniofacial and/or beak development.

"The most exciting and significant finding was that genetic variation in the ALX1 gene is associated with variation in beak shape not only between species of Darwin's finches but also among individuals of one of them, the medium ground finch," explains Leif Andersson, Uppsala University, Swedish University of Agricultural Sciences and Texas A&M University, who led the study.

"This is a very exciting discovery for us since we have previously shown that beak shape in the medium ground finch has undergone a rapid evolution in response to environmental changes. Now we know that hybridization mixes the different variants of an important gene, ALX1," says Rosemary Grant.

The ALX1 gene codes for a transcription factor with a crucial role for normal craniofacial development in vertebrates, and mutations that inactivate this gene cause severe birth defects including frontonasal dysplasia in humans.

-"This is an interesting example where mild mutations in a gene that is critical for normal development leads to phenotypic evolution," comments Leif Andersson.

"I would not be surprised if it turns out that mutations with minor or minute effects on ALX1 function or expression contribute to the bewildering facial diversity among humans," says Leif Andersson.

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When the first of the Galápagos Islands arose from the ocean floor around 3m years ago, they were naked, angry, lava-spewing cones devoid of life. Now, millions of years later, they are alive with some of the world’s most iconic animals. Giant tortoises. Sea iguanas. Flightless cormorants. And those finches equipped with Swiss army knife beaks.

The Galápagos finches are probably one of the most well-known examples of evolution and will forever be tightly linked to Charles Darwin’s voyage and his theory of natural selection (although you may be surprised to learn that the Galápagos finches were not as central to Darwin’s theory as we like to think). With their diversity of bill sizes and shapes, each species has adapted to a specific type of food; the ground-finch (Geospiza) has a thick beak adapted to feeding on a variety of crunchy seeds and arthropods, whereas the warbler finch (Certhidea olivacea) developed a slender, pointy bill to catch tasty insects hiding between the foliage. The woodpecker finch(Camarhynchus pallidus)even uses twigs or cactus spines to pry arthropods out of treeholes.

The Galápagos finches are seen as a classic example of an adaptive radiation, the rapid evolution of ecologically different species from a common ancestor. Comparisons of anatomical features of the Galápagos finches, as well as modern molecular techniques, show they are indeed more closely related to each other than to any other species. This means they form a monophyletic group, a group of organisms all descended from one ancestral species. Based on the accumulated differences that occurred in their DNA over time (a way of estimating when species split from each other), the ancestral flock likely reached the Galápagos about 2-3m years ago (Grant and Grant, 2008). What did those very first finches look like? And where did they come from?

Although many of the Galápagos Islands themselves are several million years old, the oldest known fossil remains of Galápagos finches come from the Holocene period (the last 10,000 years) (Steadman et al, 1991). These fossils are from two species of ground-finches, Geospiza nebulosi and G magnirostris, that are still living on the islands today. They thus tell us little about what the earliest finches looked like and where they might have come from.

Because of the islands’ close proximity to Ecuador, scientists have looked towards mainland South America in their search for the ancestor of the Galápagos finches. The avian palaeontologist David Steadman argued, based on morphological and behavioural similarities (1982), that the blue-back grassquit Volatinia jacarina, a small tropical bird common throughout much of Central and South America, was the most likely direct ancestor of the Galápagos finches. Later studies, such as that of Sato et al. (2001), started using mitochondrial DNA and found that another species of grassquit, Tiaris obscura, was the most likely ancestral species. This species originated in Central America, but spread into South America as the Isthmus of Panama, the land bridge between North and South America, formed around 3m years ago. From South America, it made its way to the archipelago.

However, others have argued, based on similarities in morphology as well as behaviour, that the Galápagos finches are more closely related to Caribbean species of Tiaris or the Saint Lucia black finch Melanospiza richardsoni (Baptista and Trail, 1988). This possibility of a Caribbean origin of the Galápagos finches was also corroborated by a recent analysis (Funk and Burns, 2018). In this analysis, the majority of species most closely related to the Galápagos finches were found to have their ancestral range in the Caribbean. However, the analysis was not conclusive, and there remains an equal probability of a Caribbean origin or a South American mainland origin to the Darwin’s finch radiation.

A Caribbean origin of the Galápagos finches seems counterintuitive, as the nearest mainland from the Galápagos is South America, but dispersal does not always follow a straight line. This is nicely demonstrated by the finch that inhabits nearby Cocos Island, Pinaroloxias inornata. Although this island is closer to the mainland than the Galápagos Islands themselves, genetic research has shown that the Cocos Island finch descended from a Galápagos species, not a mainland one (Grant and Grant, 2008).

Birds are excellent long-distance dispersers, even over open ocean, as demonstrated by the repeated colonisation of the Hawaiian Islands and New Zealand. Moreover, other Galápagos birds, such as mockingbirds and the Galápagos flamingo, exhibit similar Caribbean connections, indicating that a Caribbean origin is plausible. Remarkably enough, this pattern has also been found in other animal groups, such as snakes, moths and sponges (Grehan 2001). Thus the Caribbean remains as a likely source for the origin of Galápagos finches.

Although the lack of fossils means that we don’t know much about the appearance of the first finches, we can narrow down their area of origin. The closure of the Panama land bridge altered ocean circulation, and probably brought about changes in wind strength and directions. These changes may have facilitated the colonisation of the Galápagos Islands, especially if that area was the point of departure for a flock of adventurous finches.

References:

Baptista, LF, and Trail, PW, 1988. On the origin of Darwin’s finches. The Auk.

Funk, ER, and Burns, KJ, 2018. Biogeographic origins of Darwin’s finches (Thraupidae: Coerebinae). The Auk.

Grant, PR, and Grant, BR, 2008. How and Why Species Multiply: The Radiation of Darwin’s Finches. Princeton University Press, Princeton, NJ, USA.

Grehan, J, 2001. Biogeography and evolution of the Galápagos: Integration of the biological and geological evidence. Biological Journal of the Linnean Society.

Sato, A, et al., 2001. On the origin of Darwin’s finches. Molecular Biology and Evolution.

Steadman, DW, 1982. The origin of Darwin’s finches (Fringillidae, Passeriformes). Transactions of the San Diego Society of Natural History.

Steadman, DW, et al., 1991. Chronology of the Holocene Vertebrate Extinction in the Galápagos Islands. Quaternary Research.

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