The ornithologist Alfred Russel Wallace and the controversy surrounding the dinosaurian origin of birds
Over many years of his life, the British naturalist Alfred Russel Wallace (1823–1913) explored the tropical forests of Malaysia, collecting numerous specimens, including hundreds of birds, many of them new to science. Subsequently, Wallace published a series of papers on systematic ornithology, and discovered a new species on top of a volcano on Ternate, where he wrote, in 1858, his famous essay on natural selection. Based on this hands-on experience, and an analysis of an Archaeopteryx fossil, Wallace suggested that birds may have descended from dinosaurian ancestors. Here, we describe the “dinosaur-bird hypothesis” that originated with the work of Thomas H. Huxley (1825–1895). We present the strong evidence linking theropod dinosaurs to birds, and briefly outline the long and ongoing controversy around this concept. Dinosaurs preserving plumage, nesting sites and trace fossils provide overwhelming evidence for the dinosaurian origin of birds. Based on these recent findings of paleontological research, we conclude that extant birds indeed descended, with some modifications, from small, Mesozoic theropod dinosaurs. In the light of Wallace’s view of bird origins, we critically evaluate recent opposing views to this idea, including Ernst Mayr’s (1904–2005) arguments against the “dinosaur-bird hypothesis”, and document that this famous ornithologist was not correct in his assessment of this important aspect of vertebrate evolution.
KeywordsAlfred Russel WallaceEvolutionDinosaursBirdsArchaeopteryxErnst Mayr
Seven years after returning to his home country of England, Alfred Russel Wallace (1823–1913) published his most commercially successful book, The Malay Archipelago (Wallace 1869). During his 8-year-long excursions (1854–1862) into these tropical regions of planet Earth, the British naturalist independently discovered the principle of natural selection in populations of wild animals (Wallace 1858) and proposed a biogeographical concept that was later called “Wallace line”. In addition to these contributions to evolutionary biology and biogeography, he was also an avid collector and discovered/described many new species of birds.
In one of his original papers dealing with systematic ornithology, Wallace (1864) provided information on the distribution and habits of parrots of the Malayan region, with the description of two new species. In another research paper on this subject, Wallace (1865) characterized 21 species of birds from this area, and pointed out that he had, at that time, collected a total of 212 new species of birds in the islands of the Malay Archipelago.
Another of his many original contributions to ornithology dealt with the raptorial birds of the Malay Archipelago. The author remarked, “With the exception that Vultures are entirely absent, birds of prey are tolerably plentiful in the Archipelago” (Wallace 1868, p. 2). Interestingly, the British ornithologist attributed the occurrence of many species to geographic separation of populations. Hence, Wallace foresaw not only Ernst Mayr’s (1904–2005) biological species concept (Kutschera 2003, 2009), but also the principle of allopatric speciation, when he suggested that “This large number (of bird species) seems to be chiefly because of the breaking up of the district into a vast number of islands” (Wallace 1868, p. 2).
Finally, in his best- and long-seller The Malay Archipelago, Wallace (1869) devoted many pages to the distribution, behavior and taxonomy of different members of the Aves. His lucid descriptions of the exotic birds of paradise were one of the reasons for the tremendous success of this book, which is still in print today.
Alfred Russel Wallace and the origin of birds
Despite the fact that Wallace collected more than 8,000 specimens of birds and described many new species (Wallace 1869) during his travels in Southeast Asia, his writings on the evolutionary origin of birds are rather limited. His discussions of the evolutionary history of other groups are more extensive. In his popular book Darwinism, Wallace (1889) devoted chapter XIII to the “Geological evidences of evolution”. With reference to the science of geology, the author pointed out that “The theory of evolution in the organic world necessarily implies that the forms of animals and plants have, broadly speaking, progressed from a more generalized to a more specialized structure, and from simpler to more complex forms” (Wallace 1889, p. 182). Wallace discussed the evolution of horses and other animal taxa, with reference to the corresponding work of the eminent British biologist Thomas Henry Huxley (1825–1895). In one sentence, Wallace (1889) also referred to the origin of birds. In his discussion of Huxley’s research on fossil crocodiles, he remarked that “Dinosaurians (are) reptiles which in some respects approach birds” (Wallace 1889, p. 184). The author agreed with Huxley’s opinion and, on a more general note, argued that the fossil finds of his time provide “evidence of evolution; the doctrine resting upon exactly as secure a foundation as did the Copernican theory of the motions of the heavenly bodies at the time of its promulgation” (Wallace 1889, p. 187).
The dino-bird hypothesis: origin and evolution of a concept
The dinosaurian origin of birds, originating as an idea in the 1860s with Huxley (1868a, b, 1870), is widely accepted today (Prum 2002; Chiappe 2004, 2007, 2009; Erickson et al. 2009) and remains a very active and dynamic area of research. The re-emergence of the view that dinosaurs are in fact bird-like creatures is relatively recent, but first mentions of the shared anatomical characteristics between birds and (non-avian) dinosaurs, date back much further. Early pioneers of archosaur comparative anatomy, such as the German anatomist Carl Gegenbaur (1826–1903) (Hossfeld et al. 2003), and the aforementioned zoologist Huxley, recognized these similarities (Wagner 1861; Chiappe 2007), which are most apparent in the skeletons of theropod dinosaurs. Thomas H. Huxley, today widely known as “Darwin’s bulldog”, was one of the most vociferous proponents of a bird-dinosaur link (Huxley 1868a, b, 1870).
While Huxley had little doubt about the dinosaurian origin of birds, some authors considered other scenarios, such as a thecodont origin as more likely (Heilmann 1926). These views became widespread following the publication of Heilman’s influential book The Origin of Birds, aided to no small extent by the incredibly vibrant life illustrations Heilman included in this work. By the early twentieth century, dinosaurs were no longer thought to be particularly relevant to bird origins, despite the existence of a truly astonishing fossil from Europe.
Considering the huge scientific importance, beautiful preservation, and rarity of Archaeopteryx fossils, it was probably only a question of time before doubts about the authenticity of the fossil were voiced. Claims that Archaeopteryx is a forgery were quickly and thoroughly proven to be false (Charig et al. 1986), and several new specimens have been discovered (Mayr et al. 2007); they are all referred to A. lithographica by some authors (Houck et al. 1990; Senter and Robins 2003), while others distinguish two or more species (Mayr et al. 2007). For a long time, Archaeopteryx remained one of the very few physical pieces of evidence showing a mosaic of easily identifiable traditional “reptile” and “bird” characteristics.
Part of the fascination of the dinosaur-bird link undoubtedly has to do with the widespread, but superficial perception of a great difference in size and morphology between dinosaurs such as Tyrannosaurus rex and the vast majority of modern birds. In reality, many dinosaur skeletons show a striking similarity to the skeleton of a modern bird. This perception has sometimes hindered research exploring a possible relationship, and dinosaurs were generally thought to lack many typical avian features, such as a furcula, (proto) feathers, or an avian-style brooding behavior.
Fossil evidence from Asia and beyond
Of particular interest in the evolution of flight are, in addition to Archaeopteryx, several new Asian taxa, including four-winged forms such as Microraptor (Fig. 7), a small maniraptoran from Asia (Xu et al. 2003; Li et al. 2012). These new specimens add important information to our understanding of leg feather morphology and evolution (Zheng et al. 2013). The precise sequence of events leading from flightless dinosaurs to full-powered bird flight is still debated and different models have been proposed (Chiappe 2009; Dececchi and Larsson 2011). It is clear, however, that plumage did initially evolve for purposes unrelated to flight.
Frauds and unresolved questions
Unfortunately, research into the dinosaurian origin of birds has been temporarily overshadowed by examples of fraud, in particular, specimens that represent composite slabs, consisting of several taxa (Zhou et al. 2002). The most famous of these fabrications has been named “Archaeoraptor” and, because a series of unfortunate events meant that the forgery was not detected before initial description, this provided unnecessary “ammunition” to critics of the dinosaurian origin of birds, from sceptical ornithologists to US creationists. As is the case with other “Piltdown Man” style forgeries, this unfortunate episode should not detract from the fact that in the time elapsed since the “Archaeoraptor” story, countless new genuine and spectacular fossils of avian and non-avian dinosaurs have come to light, in addition to the ones already known. These new finds provide a spectacular fossil sequence, rich in diversity and morphology and indicative of a complex evolutionary branching pattern.
Because of this complexity in theropod and bird evolution, some important details of taxonomic relationships remain unresolved, as competing hypotheses are currently not strong enough to rule each other out. This is relevant to the position of certain groups of theropod dinosaurs such as dromaeosaurs, troodontids, alvarezsaurids and oviraptorids for example—all of which have at one point or another been described as theropods that are particularly close to birds, and in some cases even as secondarily flightless birds (Perle et al. 1993; Chiappe et al. 1998; Sereno 2001; Hwang et al. 2002; Paul 2002; Witmer 2002).
More recently, evolutionary developmental biology (evo-devo) has also become an important area of debate, especially regarding digit homologies. This has traditionally been a divisive and complicated issue, but data from developmental biology now seem to show little incompatibility with the theropod origin of birds (Naish 2011). This is also supported by recent studies based on molecular evidence (Vargas and Fallon 2005).
Another topic discussed in avian evolution is what some researchers refer to as the “temporal paradox” (Feduccia 1999), which, in this case, describes the temporal discrepancy between the Cretaceous age of many of the new Asian dinosaurs showing protofeathers, feathers and wings, and the appearance of the earliest known bird, Archaeopteryx, which is reliably dated to the Late Jurassic (~150 million years ago) (Fig. 3). This criticism has, however, little merit, since (a) maniraptoran dinosaurs are in fact known from remains that are early Jurassic in age and that consequently predate Archaeopteryx (e.g., Witmer 2002; Hu et al. 2009), (b) it has not been proposed that the Cretaceous forms are ancestral to Archaeopteryx or similar forms, and (c) all previously proposed alternatives are far less parsimonious (Brochu and Norell 2001; Witmer 2002).
The position of Archaeopteryx has also recently been questioned (Xu et al. 2011), because one analysis recovered the taxon outside of Aves. This result should, however, not be regarded as a major turning point. While cladistic analyses are powerful and important tools, they can suffer from a lack of data and/or stability and results obviously also depend on definitions of groups (in this case Aves). Indeed, the phylogenetic position of Archaeopteryx has subsequently been reverted back to its “original” position (Lee and Worthy 2012), emphasizing the fragility of some phylogenetic analyses, and the sometimes exaggerated importance given to them by some authors to the detriment of other approaches, such as classical comparative anatomy. This problem was the cause for several misidentifications in the past, including some concerning early birds (Naish et al. 2012; Buffetaut 2011).
Ernst Mayr and ongoing opposition against the dino-bird hypothesis
Unlike Alfred R. Wallace (1889, 1910), some modern ornithologists have opposed the dinosaurian origin of birds. This view was also espoused by one of the most influential evolutionary biologists of the twentieth century, Ernst Mayr. This world-expert in ornithology discovered and described many species of birds (Haffer 2007). In his popular book What Evolution Is, Mayr (2001), like some other ornithologists, appears to have underestimated, and possibly misunderstood some of the evidence linking theropod dinosaurs to birds.
Mayr (2001) argued that there are two distinct, plausible theories on the origin of birds, and erroneously states that the theory of the dinosaurian ancestry of birds suggests an origin from Cretaceous theropods. This is incorrect for the reasons explained above (see temporal paradox). The other theory Mayr refers to is the poorly supported thecodont origin (Witmer 2002), which suggests that birds originated from another archosaur group in the Triassic (Martin 2004). Mayr (2001) lists several, now largely discredited, lines of refutations against a dinosaurian origin of birds: differences in digit counts; differences in tooth morphology; the pectoral anatomy of late Cretaceous dinosaurs, and problems with the “ground up” model of avian flight. While a detailed refutation of the above arguments is beyond the scope of this paper and can be found elsewhere (e.g., Witmer 2002; Chiappe 2009), it is worth noting that some of them were surprisingly weak, even before the more recent discoveries described above made them untenable. To illustrate just one example, the argument that theropod teeth are more flattened than the simpler peg-like teeth of early birds (Mayr 2001) ignores the fact that theropod dentition, while often relatively similar, can also vary greatly in morphology, from conical, rounded teeth in spinosaurids (Dal Sasso et al. 2005), via the tiny, heterodont and numerous teeth of Pelecanimimus (Perez-Moreno et al. 1994), to the blade-shaped teeth of carcharodontosaurids (Sereno et al. 1996), to cite just a few examples. There is little doubt that in the face of such diversity, tooth morphology seems to be a poor choice for argument.
The view Mayr (2001) summarized in his popular book is in stark contrast to that expressed by the vast majority of vertebrate paleontologists, but emblematic for a relatively deep historical schism between the latter, and a substantial number of ornithologists (Feduccia 1999). This may be in some cases a consequence of a general lack of interest, and/or expertise, in the methods used in vertebrate paleontology. As the evidence for the dinosaurian origin of birds has continuously piled up, this divide has slowly been reduced, but it has not completely disappeared (Naish 2011). Based on currently available information and recent discoveries, the prominent ornithologist Mayr (2001) was not correct in his assessment of this particular aspect of evolutionary biology.
In two of his most influential books, Wallace (1889, 1910) discussed the evolutionary origin of birds. Based on the evidence available at that time, the ornithologist Wallace pointed out that extant birds may be the descendants of extinct dinosaurs, but he did not elaborate on this topic. This “dinobird-hypothesis” was proposed for the first time by the Victorian naturalist Thomas H. Huxley, who published several original papers on this topic (Huxley 1868a, b, 1870).
Today, it is widely accepted that birds, or “avian dinosaurs”, descended from, and in fact are, theropods that survived the Cretaceous/Paleogene mass extinction event 65 million years ago (Chiappe 2009; Kutschera 2013) (Fig. 8). Small predatory dinosaurs are the evolutionary ancestors of extant members of the Aves, a class of homoeothermic vertebrates that comprises ca. 10,000 extant species (van Tuinen 2009). Like Wallace, Ernst Mayr was a remarkable ornithologist who discovered and described numerous species of birds (Haffer 2007). However, in his influential book What Evolution Is, Mayr (2001) summarized evidence against Huxley’s “dinobird hypothesis” in its “evolved” version (Feduccia 1999).
In this article, we have shown that Mayr’s writings do not reflect the current understanding of bird origins, and conclude that these feathered vertebrates are in fact a group of highly modified theropods that evolved during the Mesozoic from small, feathered dinosaur ancestors.
The authors would like to thank Carol Abraczinskas for formatting and improving the figures, and Carol Abraczinskas and Paul Sereno for providing Fig. 8. Mick Ellison (American Museum of Natural History) kindly provided the photograph used in Fig. 7. Davide Bonadonna provided the artwork shown in Figs. 4 and 6. For comments on this manuscript, we would like to thank Alex Dececchi, Simone Maganuco and the reviewer, Daniela Schwarz-Wings.