- Email: [email protected]
Evolution: Flight of the Ratites
Current Biology
Dispatches representation in the entorhinal cortex. Science 305, 1258–1264.
12. Benhamou, S. (1996). No evidence for cognitive mapping in rats. Anim. Behav. 52, 201–212.
15. Clipperton-Allen, A., Cole, M., Peck, M., and Quirt, J. (2016). Pattern cue and visual cue competition in a foraging task by rats. Learn. Behav. 44, 378–389.
10. Taube, J.S., Muller, R.U., and Ranck, J.B. (1990). Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J. Neurosci. 10, 420–435.
13. Bicanski, A., and Burgess, N. (2016). Environmental anchoring of head direction in a computational model of retrosplenial cortex. J. Neurosci. 36, 11601–11618.
16. Iaria, G., and Burles, F. (2016). Developmental topographic disorientation. Trends Cogn. Sci. 20, 720–722.
11. Cheng, K. (1986). A purely geometric module in the rat’s spatial representation. Cognition 23, 149–178.
14. Gallistel, C.R. (1990). The Organization of Learning (Cambridge, MA: Bradford Books/ MIT Press).
17. Radiolab (2016). Lost and Found. In Radiolab. (WNYC). http://www.radiolab.org/story/ 110079-lost-found/
Evolution: Flight of the Ratites Florian Maderspacher Florian Maderspacher is Current Biology’s Senior Reviews Editor Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2016.12.023
The flightless ratite birds are scattered all across the Southern hemisphere, on landmasses that have long been separated from each other. But how did they get there? They flew in from the North.
Try to channel your inner David Attenborough voice for a moment and imagine him creeping through the shrubbery somewhere in Madagascar: ‘‘this is an elephant bird. Unable to fly, she is, if not the tallest, almost certainly the heaviest bird that ever lived on Earth, weighing nearly half a ton. And she is about to lay an equally impressive ten-kilogram egg.’’ Sadly, this is but a poor fictional rendering of an encounter that never happened. All that David Attenborough, or anyone alive today, ever got to see of the elephant bird was a bunch of bones and empty eggshells (https://www.youtube.com/ watch?v=VhIk3AW04Ck). Countless species go extinct every year, many of which remain entirely unknown. And while every species matters, sometimes the loss feels particularly tragic, when species with a truly peculiar appearance or life-style vanish. This is probably true for the enormous elephant birds — known locally as ‘vorompatras’ — or their cousins, the majestic moas of New Zealand, some of which stood over three-and-a-half meters tall. Both lineages disappeared not long after specimens of our own fine species set foot on these islands — honi soit qui
mal y pense. But imagine you could see these birds, which went extinct only a couple of centuries ago, in a zoo or in the wild (Figure 1). Imagine what formidable biology they could teach us. Moas and elephant birds are ratites, a group of bird that — paradoxically — found its evolutionary niche by abandoning the very essence of birdness, the ability to fly. With their extinction, two of the seven major ratite lineages were lost. But thanks to the ingenuity of science, moas and elephant birds, by way of DNA locked away in their bones, did give up some of their secrets and helped resolve the riddle of ratite evolution. A recent paper by Masami Hasegawa and colleagues [1] in Current Biology uses elephant bird DNA to erect the most detailed and informative family tree for the ratites yet and proposes an evolutionary scenario for how these birds lost the ability to fly, grew big and wound up on far-flung lands from Madagascar to South America. The paper nicely illustrates how current biology builds on molecular, morphological, fossil and biogeographic data combined under a phylogenetic framework to infer evolutionary scenarios that played out over tens of millions of years.
R110 Current Biology 27, R103–R122, February 6, 2017 ª 2016 Elsevier Ltd.
Rattling the Ratite Tree All living ratites are unable to fly. Freed from the constraints of having to take to the air, some ratites could grow big. The largest birds living today, the African ostrich and the Australian emu, are ratites. There are ten more living ratite species: two species of South American rhea, five species of New Zealand kiwi and three cassowary species, found in Australia and adjacent islands. The peculiar distribution of the ratites has intrigued biologists for a long time. How could flightless birds get onto these remote lands? Continental drift seemed to provide a clue: until about 150 million years ago, Africa (including Madagascar), South America, Antarctica, India, Australia and New Zealand were part of the erstwhile supercontinent Gondwana. As Gondwana broke up, the resident ratites could just have rafted along and evolved into the different clades on the different continents. Such vicariance is by no means an uncommon biogeographical pattern; it explains the distribution of many groups of plants and animals, and in fact ratites became somewhat of a poster child for Gondwanan vicariance [2,3]. Unfortunately, however, this rafting story just does not seem hold for the ratites.
Current Biology
Dispatches When evolutionary relationships are inferred from comparisons of morphological or molecular characters, the branching pattern of the resultant phylogenetic tree often hinges on the number of characters and species that are being analyzed. Inclusion of more informative traits or more groups can yield drastically different evolutionary trees. That’s what happened with the ratites. With the extinction of moas and elephant birds, two major ratite lineages (and possibly more than half of all ratite species) had gone missing. But once it became possible to retrieve DNA from long dead organisms, these extinct ratites could be placed in the evolutionary tree, leading to major upsets. When DNA sequences from moas were use to place them in the ratite tree, it turned out that their closest relatives are not — as one might have expected — their local neighbors, the kiwis, but instead the partridge-like South American tinamous [4]. However, tinamous, of which there are over 40 species, are not ratites. They have long been known to be close relatives of ratites: based on the common anatomy of their palates ratites and tinamous, together with some fossil birds, make up the paleognath (‘old-jaw’) birds, which are distinct from all other living birds, the neognaths. This surprising placement of tinamous within ratites, next to moas, meant that the ratites no longer were a monophyletic group. Hence, there never was a bird that was the common ancestor to all ratites and only the ratites. In that sense, they differ from the other major flightless bird group, the penguins, which are monophyletic and diversified from a flightless common ancestor [5]. The real puzzle, however, is that tinamous are able to fly. If tinamous are deeply nested within ratites, then either tinamous must have re-gained flight ability after the ancestor of all living paleognaths had lost it, or the different ratite lineages must have lost the ability to fly independently [6,7]. That a flightless bird should re-evolve flight is highly unlikely. Such evolutionary reversals are exceedingly rare according to ‘Dollo’s law’, which states that traits once lost in evolution do not come back. Independent flight losses are more likely, as it is conceivably much easier to lose the ability to fly than to gain it. Flying is energetically
costly, and thus, if not forced by the circumstances, such as predators or competitors, birds seem quite happy to give it up altogether. In fact, flight has been lost in a large number of bird species, from over a dozen different families. The poster child of these is the Dodo, a pigeon-relative that lived on Mauritius. Like the dodo, most of the flightless bird species were endemic to remote, predator-free islands, and like the dodo, many are extinct now. Ancestors of the different ratite lineages appear to have lost the ability to fly independently of each other in parallel, at least three times [6]. But if flightlessness is so rampant among the paleognaths, what was it about these birds that predisposed them to abandoning the air so readily? One possibility is the adaptation to a largely ground-dwelling life-style still seen in today’s tinamous. Ratite Revelations The fact that the closest relative of the New Zealand moas is a group of bird in distant South America also cast doubt on the vicariance scenario. And the picture became even more puzzling when mitochondrial DNA from the ancient elephant birds was analyzed and compared to that of other paleognaths. It turned out that the closest relatives of the enormous elephant birds are the humble kiwis [8]. However, Madagascar and New Zealand never were particularly close together and have been on separate landmasses for nearly 150 million years. Now, Hasegawa and colleagues [1] may well have put the final nail into the coffin of the vicariance scenario. They have managed to get hold of large portions of the nuclear genome (not just mitochondrial DNA) from elephant bird remains. Reassuringly, they recover the same basic structure of the paleognath evolutionary tree, including the close relationship between elephant birds and kiwis (Figure 2). To infer evolutionary processes, however, the evolutionary tree’s branching pattern alone often does not suffice. The various divergences need to be timed so they can be related to historical occurrences, such as changes in geography or climate, that might have driven evolutionary processes. Time is integrated into evolutionary trees in two fundamental ways [9]: through genetic
Figure 1. Imagining the vorompatra. All that is left of what was once Earth’s largest bird, the Malagasy giant elephant bird or vorompatra, are bones and eggshells. It remains for artists to image what they may have looked like. Here, Walton Ford conjured up an image of this bird, already in the ties of humans who would eventually lead to its demise. Image courtesy of the artist and Paul Kasmin Gallery.
divergences, which give the relative ages of the branching events in the tree, and through fossil calibrations, which provide absolute ages for some branching events. Through the integration of both, age estimates can be assigned to all the crucial branching points in the evolutionary tree. Most major divergence events in the ratite tree erected by Hasegawa and colleagues [1] took place between 70 and 60 million years ago (Figure 2), although the particular order in which clades split from each other is less clear, because some of these higher-level groupings (as well as the precise position of the rheas in the tree) are less strongly supported. That these divergence times coincide with the mass extinction at the end of the Cretaceous is no coincidence. In fact, many other groups of bird are seen to diverge around that time [10,11]. The
Current Biology 27, R103–R122, February 6, 2017 R111
Current Biology
Dispatches Diversification
Spread
Elephant birds Kiwis Emu
Northern origins
Cassowaries
Southern dispersal
Tinamous Moas Rheas Ostrich Lithornis cohort Current Biology
Figure 2. Paleognath phylogeny and evolution. Based on their timed phylogeny, Hasegawa and colleagues [1] formulate a new three-phase scenario for the evolution of ratite (and paleognath) birds. Paleognaths originated in the Northern hemisphere during the late Early Cretaceous (115–105 million years ago). Between 70 and 80 million years ago, the ancestors of all extant paleognaths — except the ostrich which came to Africa from Eurasia — spread into the Southern hemisphere via South America. In the wake of the late Cretaceous mass extinction that wiped out the dinosaurs, they diversified and — via the Southern continent of Antarctica, which was temperate and not yet the ice desert it turned into some 35 million years ago — dispersed by air into various Gondwanan fragment lands, such as Australia, New Zealand or Madagascar, where they independently lost the ability to fly and, with the exception of the kiwis, grew big. (Silhouettes of emu, elephant bird, ostrich, tinamous and rhea by Darren Naish (vectorize by T. Michael Keesey)).
annihilation of the dinosaurs, which occupied nearly every major ecological niche in the Mesozoic world, had left ample opportunity for new forms to take their place. And unlike mammals, which remained small for another 10 million years or so, birds jumped at the occasion. Giant birds emerged, like Gastornis in the Northern Hemisphere or the phorusrhacid ‘terror birds’ in South America. And ratites may have similarly filled the niche left empty by the dinosaurs. This may also explain why — unlike many of the islanddwelling flightless birds that went extinct as soon as mammals (mostly rats) arrived — flightless ratites managed to prevail even in places like Africa or Australia where many mammals were present. They simply may have gotten there first and evolved a large body that set them apart from the competition [8]. Some insight about when ratites lost the ability to fly and became big can be gleaned also from the molecular data used to build the phylogeny. Hasegawa and colleagues [1] find that the inferred rates of molecular evolution at the base of the paleognath tree are consistent with the ancestral paleognaths weighing between four and five kilograms and being able to fly. Such inferences are possible, because the rate with which mitochondrial DNA evolves has been
demonstrated to be higher in birds that are able to fly than in flightless birds (possibly due to the higher metabolic load of flight) and is negatively correlated with body size [12]. But of course they hinge on the historic rates of evolution being inferred correctly. Ultimately, a complete picture of the evolution of a group of animals like the ratites needs to also include their long-lost potential ancestors and relatives. As no DNA is available for such species, known only from often incomplete fossils, they need to be placed in the evolutionary tree based on morphological characters. However, a morphology-based phylogeny is tricky for the ratites, where flightlessness and the morphological adaptations that come with it may have evolved several times in parallel. As such homoplasic traits may suggest spurious evolutionary relationships, Hasegawa and colleagues [1] relied on their molecular phylogeny to identify and exclude such traits, and erect an evolutionary tree of paleognaths based on more reliable morphology. This tree includes a loose group of fossil birds, referred to as the ‘Lithornis-cohort’, after Lithornis, one of the first fossil birds to be found [13]. In the new phylogeny, Lithornis and associates consistently occupy a basal position in the tree [1,14],
R112 Current Biology 27, R103–R122, February 6, 2017
suggesting that ratites may have evolved from a Lithornis-like bird. It is clear from their fossils that these birds could fly, but more strikingly, they all come from the Northern hemisphere, leading Hasegawa and colleagues [1] to suggest that the ratite ancestors also originated in the North. Fitting with this idea, the first ratite lineage to branch, the ostrich lineage, was initially widely distributed in Eurasia and entered Africa only after contact was established. Between 70 and 80 million years ago, the ancestors of all other ratites and the tinamous entered the Southern hemisphere, presumably via South America. After the dinosaur extinction, these birds diversified and — presumably with the then ice-free Antarctica as a hub — flew into Madagascar, Australia and New Zealand, where they independently lost the ability to fly and grew big. How could this evolutionary scenario be tested? Once more, the answers will have to come from extinct creatures, in the form of fossils. And it may in fact be the current human-made extinction crisis, with its changing climate, that might melt the ice in parts of Antarctica and liberate the remains of ratite ancestors. What an irony that would be. REFERENCES 1. Yonezawa, T., Segawa, T., Mori, H., Campos, P.F., Hongoh, Y., Endo, H., Akiyoshi, A., Kohno, N., Nishida, S., Wu, J., et al. (2017). Phylogenomics and morphology of extinct paleognaths reveal the origin and evolution of the ratites. Curr. Biol. 27, 68–77. 2. Cracraft, J. (1974). Phylogeny and evolution of the ratite birds. Ibis 116, 494–521. 3. Cracraft, J. (2001). Avian evolution, Gondwana biogeography and the Cretaceous-Tertiary mass extinction event. Proc. R. Soc. B 268, 459–469. 4. Phillips, M.J., Gibb, G.C., Crimp, E.A., and Penny, D. (2009). Tinamous and moa flock together: mitochondrial genome Sequence analysis reveals independent losses of flight among ratites. Syst. Biol. 59, 90–107. 5. Gavryushkina, A., Heath, T.A., Ksepka, D.T., Stadler, T., Welch, D., and Drummond, A.J. (2016). Bayesian total-evidence dating reveals the recent crown radiation of penguins. Syst. Biol. http://dx.doi.org/10.1093/sysbio/ syw060. 6. Harshman, J., Braun, E.L., Braun, M.J., Huddleston, C.J., Bowie, R.C.K., Chojnowski, J.L., Hackett, S.J., Han, K.-L., Kimball, R.T., Marks, B.D., et al. (2008). Phylogenomic evidence for multiple losses of flight in ratite birds. Proc. Natl. Acad. Sci. USA 105, 13462– 13467.
Current Biology
Dispatches 7. Baker, A.J., Haddrath, O., McPherson, J.D., and Cloutier, A. (2014). Genomic support for a moa-tinamou clade and adaptive morphological convergence in flightless ratites. Mol. Biol. Evol. 31, 1686–1696. 8. Mitchell, K.J., Llamas, B., Soubrier, J., Rawlence, N.J., Worthy, T.H., Wood, J., Lee, M.S., and Cooper, A. (2014). Ancient DNA reveals elephant birds and kiwi are sister taxa and clarifies ratite bird evolution. Science 344, 898–900. 9. Lee, M.S.Y., and Ho, S.Y.W. (2016). Molecular clocks. Curr. Biol. 26, R399–R402.
10. Jarvis, E.D., Mirarab, S., Aberer, A.J., Li, B., Houde, P., Li, C., Ho, S.Y., Faircloth, B.C., Nabholz, B., Howard, J.T., et al. (2014). Wholegenome analyses resolve early branches in the tree of life of modern birds. Science 346, 1320– 1331. 11. Prum, R.O., Berv, J.S., Dornburg, A., Field, D.J., Townsend, J.P., Moriarty Lemmon, E., and Lemmon, A.R. (2015). A comprehensive phylogeny of birds (Aves) using targeted nextgeneration DNA sequencing. Nature 526, 569–573. 12. Lartillot, N., and Poujol, R. (2011). A phylogenetic model for investigating
correlated evolution of substitution rates and continuous phenotypic characters. Mol. Biol. Evol. 28, 729–744. 13. Houde, P. (1986). Ancestors of ostriches found in the Northern Hemisphere suggest a new hypothesis for origin of ratites. Nature 324, 563–565. 14. Nesbitt, S.J., and Clarke, J.A. (2016). The anatomy and taxonomy of the exquisitely preserved Green River Formation (Early Eocene) lithornithids (Aves) and the Relationships of Lithornithidae. Bull. Am. Mus. Nat. Hist. 406, 1–91.
Insect Evolution: The Origin of Wings Andrew Ross Department of Natural Sciences, National Museum of Scotland, Chambers Street, Edinburgh EH1 1JF, UK Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2016.12.014
The debate on the evolution of wings in insects has reached a new level. The study of primitive fossil insect nymphs has revealed that wings developed from a combination of the dorsal part of the thorax and the body wall. How animals acquired the ability to fly is a question of major interest to evolutionary biologists. Flight enables an animal to disperse across physical barriers, such as seas, live in comparatively safe places away from ground-dwelling predators, to access food sources that others cannot reach and to find a mate. Vertebrates evolved the ability for powered flight independently in several lineages, such as pterosaurs, birds and bats. However, the insects got there first and it is widely believed that they evolved wings and the ability to fly only once. A recent paper in Current Biology by Prokop et al. [1] has taken the long discussion of the origin of wings and flight in insects to the next level. The debate on the subject goes back to the 19th century when there were two main positions on the origin of insect wings, namely whether they developed as entirely new structures or from preexisting structures. As the latter gained acceptance, the discussion moved on to which structures, either tracheal gills (like those of mayfly nymphs) or paranota (lateral extensions of the nota, the dorsal part of thoracic body segments). The latter idea received support when
Lithomantis carbonarius, one of the first articulated Carboniferous fossil insects, was discovered (Figure 1A) [2]. This species belongs to the extinct order Palaeodictyoptera, which is widely regarded as the most primitive group of winged insects. Its oldest known fossil representative (the oldest known winged insect), is the 325 million year old Delitzschala bitterfeldensis [3]. Palaeodictyoptera had their heyday in the Carboniferous and rapidly diversified into over 30 families though had become extinct by the end of the Permian (252 million years ago) [4]. They had a pointed beak for piercing and it is believed they fed on fluids from the seeds and stems of giant clubmosses and tree ferns, as holes of the right size have been found in fossils [5]. Palaeodictyoptera possessed two pairs of outstretched wings and veined paranotal lobes on the prothorax as can been seen on L. carbonarius. Thus the paranotal theory gained acceptance [6], though the tracheal gill theory did not go away and was championed by others later [7]. In the first half of the 20th century, there were two main theories for the origin of
flight in insects, the ‘flying squirrel’ and ‘flying fish’ theories depending on whether the author believed flight originated on land (by launching off giant clubmosses) or from the surface of the sea. Both hypothesised that the extended paranotal lobes enabled the insect to glide, then to steer and finally to flap [8]. The ‘flying squirrel’ model became the generally accepted norm, particularly supported by the discovery of the then oldest known fossil ‘insect’, the 407 million year old springtail Rhyniella praecursor preserved in Rhynie Chert. The chert was deposited by hot volcanic springs and preserved the earliest known terrestrial ecosystem [9]. Springtails (Collembola) are wingless and have six legs (hexapods, like all insects) and today they, along with some other apterygotes (diplurans and proturans), are regarded as the sister group to the Insecta because they have internal rather than external mouthparts. Springtails have a unique structure, the furcula (spring) that they use to propel themselves into the air to escape hazardous situations. The furcula can be seen on Rhyniella [10] (Figure 1B). So even though springtails were the first to experience the wind
Current Biology 27, R103–R122, February 6, 2017 ª 2016 Elsevier Ltd. R113
Dispatches representation in the entorhinal cortex. Science 305, 1258–1264.
12. Benhamou, S. (1996). No evidence for cognitive mapping in rats. Anim. Behav. 52, 201–212.
15. Clipperton-Allen, A., Cole, M., Peck, M., and Quirt, J. (2016). Pattern cue and visual cue competition in a foraging task by rats. Learn. Behav. 44, 378–389.
10. Taube, J.S., Muller, R.U., and Ranck, J.B. (1990). Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J. Neurosci. 10, 420–435.
13. Bicanski, A., and Burgess, N. (2016). Environmental anchoring of head direction in a computational model of retrosplenial cortex. J. Neurosci. 36, 11601–11618.
16. Iaria, G., and Burles, F. (2016). Developmental topographic disorientation. Trends Cogn. Sci. 20, 720–722.
11. Cheng, K. (1986). A purely geometric module in the rat’s spatial representation. Cognition 23, 149–178.
14. Gallistel, C.R. (1990). The Organization of Learning (Cambridge, MA: Bradford Books/ MIT Press).
17. Radiolab (2016). Lost and Found. In Radiolab. (WNYC). http://www.radiolab.org/story/ 110079-lost-found/
Evolution: Flight of the Ratites Florian Maderspacher Florian Maderspacher is Current Biology’s Senior Reviews Editor Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2016.12.023
The flightless ratite birds are scattered all across the Southern hemisphere, on landmasses that have long been separated from each other. But how did they get there? They flew in from the North.
Try to channel your inner David Attenborough voice for a moment and imagine him creeping through the shrubbery somewhere in Madagascar: ‘‘this is an elephant bird. Unable to fly, she is, if not the tallest, almost certainly the heaviest bird that ever lived on Earth, weighing nearly half a ton. And she is about to lay an equally impressive ten-kilogram egg.’’ Sadly, this is but a poor fictional rendering of an encounter that never happened. All that David Attenborough, or anyone alive today, ever got to see of the elephant bird was a bunch of bones and empty eggshells (https://www.youtube.com/ watch?v=VhIk3AW04Ck). Countless species go extinct every year, many of which remain entirely unknown. And while every species matters, sometimes the loss feels particularly tragic, when species with a truly peculiar appearance or life-style vanish. This is probably true for the enormous elephant birds — known locally as ‘vorompatras’ — or their cousins, the majestic moas of New Zealand, some of which stood over three-and-a-half meters tall. Both lineages disappeared not long after specimens of our own fine species set foot on these islands — honi soit qui
mal y pense. But imagine you could see these birds, which went extinct only a couple of centuries ago, in a zoo or in the wild (Figure 1). Imagine what formidable biology they could teach us. Moas and elephant birds are ratites, a group of bird that — paradoxically — found its evolutionary niche by abandoning the very essence of birdness, the ability to fly. With their extinction, two of the seven major ratite lineages were lost. But thanks to the ingenuity of science, moas and elephant birds, by way of DNA locked away in their bones, did give up some of their secrets and helped resolve the riddle of ratite evolution. A recent paper by Masami Hasegawa and colleagues [1] in Current Biology uses elephant bird DNA to erect the most detailed and informative family tree for the ratites yet and proposes an evolutionary scenario for how these birds lost the ability to fly, grew big and wound up on far-flung lands from Madagascar to South America. The paper nicely illustrates how current biology builds on molecular, morphological, fossil and biogeographic data combined under a phylogenetic framework to infer evolutionary scenarios that played out over tens of millions of years.
R110 Current Biology 27, R103–R122, February 6, 2017 ª 2016 Elsevier Ltd.
Rattling the Ratite Tree All living ratites are unable to fly. Freed from the constraints of having to take to the air, some ratites could grow big. The largest birds living today, the African ostrich and the Australian emu, are ratites. There are ten more living ratite species: two species of South American rhea, five species of New Zealand kiwi and three cassowary species, found in Australia and adjacent islands. The peculiar distribution of the ratites has intrigued biologists for a long time. How could flightless birds get onto these remote lands? Continental drift seemed to provide a clue: until about 150 million years ago, Africa (including Madagascar), South America, Antarctica, India, Australia and New Zealand were part of the erstwhile supercontinent Gondwana. As Gondwana broke up, the resident ratites could just have rafted along and evolved into the different clades on the different continents. Such vicariance is by no means an uncommon biogeographical pattern; it explains the distribution of many groups of plants and animals, and in fact ratites became somewhat of a poster child for Gondwanan vicariance [2,3]. Unfortunately, however, this rafting story just does not seem hold for the ratites.
Current Biology
Dispatches When evolutionary relationships are inferred from comparisons of morphological or molecular characters, the branching pattern of the resultant phylogenetic tree often hinges on the number of characters and species that are being analyzed. Inclusion of more informative traits or more groups can yield drastically different evolutionary trees. That’s what happened with the ratites. With the extinction of moas and elephant birds, two major ratite lineages (and possibly more than half of all ratite species) had gone missing. But once it became possible to retrieve DNA from long dead organisms, these extinct ratites could be placed in the evolutionary tree, leading to major upsets. When DNA sequences from moas were use to place them in the ratite tree, it turned out that their closest relatives are not — as one might have expected — their local neighbors, the kiwis, but instead the partridge-like South American tinamous [4]. However, tinamous, of which there are over 40 species, are not ratites. They have long been known to be close relatives of ratites: based on the common anatomy of their palates ratites and tinamous, together with some fossil birds, make up the paleognath (‘old-jaw’) birds, which are distinct from all other living birds, the neognaths. This surprising placement of tinamous within ratites, next to moas, meant that the ratites no longer were a monophyletic group. Hence, there never was a bird that was the common ancestor to all ratites and only the ratites. In that sense, they differ from the other major flightless bird group, the penguins, which are monophyletic and diversified from a flightless common ancestor [5]. The real puzzle, however, is that tinamous are able to fly. If tinamous are deeply nested within ratites, then either tinamous must have re-gained flight ability after the ancestor of all living paleognaths had lost it, or the different ratite lineages must have lost the ability to fly independently [6,7]. That a flightless bird should re-evolve flight is highly unlikely. Such evolutionary reversals are exceedingly rare according to ‘Dollo’s law’, which states that traits once lost in evolution do not come back. Independent flight losses are more likely, as it is conceivably much easier to lose the ability to fly than to gain it. Flying is energetically
costly, and thus, if not forced by the circumstances, such as predators or competitors, birds seem quite happy to give it up altogether. In fact, flight has been lost in a large number of bird species, from over a dozen different families. The poster child of these is the Dodo, a pigeon-relative that lived on Mauritius. Like the dodo, most of the flightless bird species were endemic to remote, predator-free islands, and like the dodo, many are extinct now. Ancestors of the different ratite lineages appear to have lost the ability to fly independently of each other in parallel, at least three times [6]. But if flightlessness is so rampant among the paleognaths, what was it about these birds that predisposed them to abandoning the air so readily? One possibility is the adaptation to a largely ground-dwelling life-style still seen in today’s tinamous. Ratite Revelations The fact that the closest relative of the New Zealand moas is a group of bird in distant South America also cast doubt on the vicariance scenario. And the picture became even more puzzling when mitochondrial DNA from the ancient elephant birds was analyzed and compared to that of other paleognaths. It turned out that the closest relatives of the enormous elephant birds are the humble kiwis [8]. However, Madagascar and New Zealand never were particularly close together and have been on separate landmasses for nearly 150 million years. Now, Hasegawa and colleagues [1] may well have put the final nail into the coffin of the vicariance scenario. They have managed to get hold of large portions of the nuclear genome (not just mitochondrial DNA) from elephant bird remains. Reassuringly, they recover the same basic structure of the paleognath evolutionary tree, including the close relationship between elephant birds and kiwis (Figure 2). To infer evolutionary processes, however, the evolutionary tree’s branching pattern alone often does not suffice. The various divergences need to be timed so they can be related to historical occurrences, such as changes in geography or climate, that might have driven evolutionary processes. Time is integrated into evolutionary trees in two fundamental ways [9]: through genetic
Figure 1. Imagining the vorompatra. All that is left of what was once Earth’s largest bird, the Malagasy giant elephant bird or vorompatra, are bones and eggshells. It remains for artists to image what they may have looked like. Here, Walton Ford conjured up an image of this bird, already in the ties of humans who would eventually lead to its demise. Image courtesy of the artist and Paul Kasmin Gallery.
divergences, which give the relative ages of the branching events in the tree, and through fossil calibrations, which provide absolute ages for some branching events. Through the integration of both, age estimates can be assigned to all the crucial branching points in the evolutionary tree. Most major divergence events in the ratite tree erected by Hasegawa and colleagues [1] took place between 70 and 60 million years ago (Figure 2), although the particular order in which clades split from each other is less clear, because some of these higher-level groupings (as well as the precise position of the rheas in the tree) are less strongly supported. That these divergence times coincide with the mass extinction at the end of the Cretaceous is no coincidence. In fact, many other groups of bird are seen to diverge around that time [10,11]. The
Current Biology 27, R103–R122, February 6, 2017 R111
Current Biology
Dispatches Diversification
Spread
Elephant birds Kiwis Emu
Northern origins
Cassowaries
Southern dispersal
Tinamous Moas Rheas Ostrich Lithornis cohort Current Biology
Figure 2. Paleognath phylogeny and evolution. Based on their timed phylogeny, Hasegawa and colleagues [1] formulate a new three-phase scenario for the evolution of ratite (and paleognath) birds. Paleognaths originated in the Northern hemisphere during the late Early Cretaceous (115–105 million years ago). Between 70 and 80 million years ago, the ancestors of all extant paleognaths — except the ostrich which came to Africa from Eurasia — spread into the Southern hemisphere via South America. In the wake of the late Cretaceous mass extinction that wiped out the dinosaurs, they diversified and — via the Southern continent of Antarctica, which was temperate and not yet the ice desert it turned into some 35 million years ago — dispersed by air into various Gondwanan fragment lands, such as Australia, New Zealand or Madagascar, where they independently lost the ability to fly and, with the exception of the kiwis, grew big. (Silhouettes of emu, elephant bird, ostrich, tinamous and rhea by Darren Naish (vectorize by T. Michael Keesey)).
annihilation of the dinosaurs, which occupied nearly every major ecological niche in the Mesozoic world, had left ample opportunity for new forms to take their place. And unlike mammals, which remained small for another 10 million years or so, birds jumped at the occasion. Giant birds emerged, like Gastornis in the Northern Hemisphere or the phorusrhacid ‘terror birds’ in South America. And ratites may have similarly filled the niche left empty by the dinosaurs. This may also explain why — unlike many of the islanddwelling flightless birds that went extinct as soon as mammals (mostly rats) arrived — flightless ratites managed to prevail even in places like Africa or Australia where many mammals were present. They simply may have gotten there first and evolved a large body that set them apart from the competition [8]. Some insight about when ratites lost the ability to fly and became big can be gleaned also from the molecular data used to build the phylogeny. Hasegawa and colleagues [1] find that the inferred rates of molecular evolution at the base of the paleognath tree are consistent with the ancestral paleognaths weighing between four and five kilograms and being able to fly. Such inferences are possible, because the rate with which mitochondrial DNA evolves has been
demonstrated to be higher in birds that are able to fly than in flightless birds (possibly due to the higher metabolic load of flight) and is negatively correlated with body size [12]. But of course they hinge on the historic rates of evolution being inferred correctly. Ultimately, a complete picture of the evolution of a group of animals like the ratites needs to also include their long-lost potential ancestors and relatives. As no DNA is available for such species, known only from often incomplete fossils, they need to be placed in the evolutionary tree based on morphological characters. However, a morphology-based phylogeny is tricky for the ratites, where flightlessness and the morphological adaptations that come with it may have evolved several times in parallel. As such homoplasic traits may suggest spurious evolutionary relationships, Hasegawa and colleagues [1] relied on their molecular phylogeny to identify and exclude such traits, and erect an evolutionary tree of paleognaths based on more reliable morphology. This tree includes a loose group of fossil birds, referred to as the ‘Lithornis-cohort’, after Lithornis, one of the first fossil birds to be found [13]. In the new phylogeny, Lithornis and associates consistently occupy a basal position in the tree [1,14],
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suggesting that ratites may have evolved from a Lithornis-like bird. It is clear from their fossils that these birds could fly, but more strikingly, they all come from the Northern hemisphere, leading Hasegawa and colleagues [1] to suggest that the ratite ancestors also originated in the North. Fitting with this idea, the first ratite lineage to branch, the ostrich lineage, was initially widely distributed in Eurasia and entered Africa only after contact was established. Between 70 and 80 million years ago, the ancestors of all other ratites and the tinamous entered the Southern hemisphere, presumably via South America. After the dinosaur extinction, these birds diversified and — presumably with the then ice-free Antarctica as a hub — flew into Madagascar, Australia and New Zealand, where they independently lost the ability to fly and grew big. How could this evolutionary scenario be tested? Once more, the answers will have to come from extinct creatures, in the form of fossils. And it may in fact be the current human-made extinction crisis, with its changing climate, that might melt the ice in parts of Antarctica and liberate the remains of ratite ancestors. What an irony that would be. REFERENCES 1. Yonezawa, T., Segawa, T., Mori, H., Campos, P.F., Hongoh, Y., Endo, H., Akiyoshi, A., Kohno, N., Nishida, S., Wu, J., et al. (2017). Phylogenomics and morphology of extinct paleognaths reveal the origin and evolution of the ratites. Curr. Biol. 27, 68–77. 2. Cracraft, J. (1974). Phylogeny and evolution of the ratite birds. Ibis 116, 494–521. 3. Cracraft, J. (2001). Avian evolution, Gondwana biogeography and the Cretaceous-Tertiary mass extinction event. Proc. R. Soc. B 268, 459–469. 4. Phillips, M.J., Gibb, G.C., Crimp, E.A., and Penny, D. (2009). Tinamous and moa flock together: mitochondrial genome Sequence analysis reveals independent losses of flight among ratites. Syst. Biol. 59, 90–107. 5. Gavryushkina, A., Heath, T.A., Ksepka, D.T., Stadler, T., Welch, D., and Drummond, A.J. (2016). Bayesian total-evidence dating reveals the recent crown radiation of penguins. Syst. Biol. http://dx.doi.org/10.1093/sysbio/ syw060. 6. Harshman, J., Braun, E.L., Braun, M.J., Huddleston, C.J., Bowie, R.C.K., Chojnowski, J.L., Hackett, S.J., Han, K.-L., Kimball, R.T., Marks, B.D., et al. (2008). Phylogenomic evidence for multiple losses of flight in ratite birds. Proc. Natl. Acad. Sci. USA 105, 13462– 13467.
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Dispatches 7. Baker, A.J., Haddrath, O., McPherson, J.D., and Cloutier, A. (2014). Genomic support for a moa-tinamou clade and adaptive morphological convergence in flightless ratites. Mol. Biol. Evol. 31, 1686–1696. 8. Mitchell, K.J., Llamas, B., Soubrier, J., Rawlence, N.J., Worthy, T.H., Wood, J., Lee, M.S., and Cooper, A. (2014). Ancient DNA reveals elephant birds and kiwi are sister taxa and clarifies ratite bird evolution. Science 344, 898–900. 9. Lee, M.S.Y., and Ho, S.Y.W. (2016). Molecular clocks. Curr. Biol. 26, R399–R402.
10. Jarvis, E.D., Mirarab, S., Aberer, A.J., Li, B., Houde, P., Li, C., Ho, S.Y., Faircloth, B.C., Nabholz, B., Howard, J.T., et al. (2014). Wholegenome analyses resolve early branches in the tree of life of modern birds. Science 346, 1320– 1331. 11. Prum, R.O., Berv, J.S., Dornburg, A., Field, D.J., Townsend, J.P., Moriarty Lemmon, E., and Lemmon, A.R. (2015). A comprehensive phylogeny of birds (Aves) using targeted nextgeneration DNA sequencing. Nature 526, 569–573. 12. Lartillot, N., and Poujol, R. (2011). A phylogenetic model for investigating
correlated evolution of substitution rates and continuous phenotypic characters. Mol. Biol. Evol. 28, 729–744. 13. Houde, P. (1986). Ancestors of ostriches found in the Northern Hemisphere suggest a new hypothesis for origin of ratites. Nature 324, 563–565. 14. Nesbitt, S.J., and Clarke, J.A. (2016). The anatomy and taxonomy of the exquisitely preserved Green River Formation (Early Eocene) lithornithids (Aves) and the Relationships of Lithornithidae. Bull. Am. Mus. Nat. Hist. 406, 1–91.
Insect Evolution: The Origin of Wings Andrew Ross Department of Natural Sciences, National Museum of Scotland, Chambers Street, Edinburgh EH1 1JF, UK Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2016.12.014
The debate on the evolution of wings in insects has reached a new level. The study of primitive fossil insect nymphs has revealed that wings developed from a combination of the dorsal part of the thorax and the body wall. How animals acquired the ability to fly is a question of major interest to evolutionary biologists. Flight enables an animal to disperse across physical barriers, such as seas, live in comparatively safe places away from ground-dwelling predators, to access food sources that others cannot reach and to find a mate. Vertebrates evolved the ability for powered flight independently in several lineages, such as pterosaurs, birds and bats. However, the insects got there first and it is widely believed that they evolved wings and the ability to fly only once. A recent paper in Current Biology by Prokop et al. [1] has taken the long discussion of the origin of wings and flight in insects to the next level. The debate on the subject goes back to the 19th century when there were two main positions on the origin of insect wings, namely whether they developed as entirely new structures or from preexisting structures. As the latter gained acceptance, the discussion moved on to which structures, either tracheal gills (like those of mayfly nymphs) or paranota (lateral extensions of the nota, the dorsal part of thoracic body segments). The latter idea received support when
Lithomantis carbonarius, one of the first articulated Carboniferous fossil insects, was discovered (Figure 1A) [2]. This species belongs to the extinct order Palaeodictyoptera, which is widely regarded as the most primitive group of winged insects. Its oldest known fossil representative (the oldest known winged insect), is the 325 million year old Delitzschala bitterfeldensis [3]. Palaeodictyoptera had their heyday in the Carboniferous and rapidly diversified into over 30 families though had become extinct by the end of the Permian (252 million years ago) [4]. They had a pointed beak for piercing and it is believed they fed on fluids from the seeds and stems of giant clubmosses and tree ferns, as holes of the right size have been found in fossils [5]. Palaeodictyoptera possessed two pairs of outstretched wings and veined paranotal lobes on the prothorax as can been seen on L. carbonarius. Thus the paranotal theory gained acceptance [6], though the tracheal gill theory did not go away and was championed by others later [7]. In the first half of the 20th century, there were two main theories for the origin of
flight in insects, the ‘flying squirrel’ and ‘flying fish’ theories depending on whether the author believed flight originated on land (by launching off giant clubmosses) or from the surface of the sea. Both hypothesised that the extended paranotal lobes enabled the insect to glide, then to steer and finally to flap [8]. The ‘flying squirrel’ model became the generally accepted norm, particularly supported by the discovery of the then oldest known fossil ‘insect’, the 407 million year old springtail Rhyniella praecursor preserved in Rhynie Chert. The chert was deposited by hot volcanic springs and preserved the earliest known terrestrial ecosystem [9]. Springtails (Collembola) are wingless and have six legs (hexapods, like all insects) and today they, along with some other apterygotes (diplurans and proturans), are regarded as the sister group to the Insecta because they have internal rather than external mouthparts. Springtails have a unique structure, the furcula (spring) that they use to propel themselves into the air to escape hazardous situations. The furcula can be seen on Rhyniella [10] (Figure 1B). So even though springtails were the first to experience the wind
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