No new thing under the sun? Finding sunbird species in Wallacea

A male Wakatobi Sunbird

Our understanding of how species interact and evolve depends on accurate knowledge of the species that exist on Earth. There are still many species to be identified, however, even in evolutionarily significant regions such as Wallacea in central Indonesia, site of Alfred Russel Wallace’s pioneering work. Our new paper, completed jointly with researchers from Universitas Halu Oleo and just published in the Zoological Journal of the Linnean Society, draws on work carried out in Wallacea to identify multiple unrecognised species in the beautiful sunbird family. Made using modern genetic, acoustic, and statistical techniques, these discoveries add to our understanding of how life evolved in this region and reinforce some of Wallace’s original ideas.

The key discovery is the “Wakatobi Sunbird Cinnyris infrenatus”, a species endemic to the small islands of the Wakatobi archipelago, off Southeast Sulawesi in central Indonesia. The Wakatobi Islands have been separated from other landmasses since they first rose out of the sea, and so there has been plenty of time for their populations to evolve in isolation and produce endemic taxa, found nowhere else on Earth. The Wakatobi Islands have been recognised as a Key Biodiversity Area for their importance to the survival of biodiversity. The Wakatobi Sunbird is the latest endemic species to be identified by our research group, following previous work on the Wakatobi Flowerpecker and the double discovery of the Wakatobi White-eye and Wangi-wangi White-eye. It’s important that we know all of the species of Southeast Sulawesi and the Wakatobi Islands, because this region acts as a “natural laboratory” for the study of evolutionary processes such as cryptic sexual dimorphism, the “supertramp strategy”, and the links between behaviour and population divergence. The Wakatobi Sunbird is currently treated as a subspecies of the widespread Olive-backed Sunbird (Cinnyris jugularis), but our findings indicate that the Olive-backed Sunbird is actually made up of at least 4 reproductively isolated species.

The sunbirds (Nectariniidae) fill a similar niche in Africa, Asia, and Australia to the hummingbirds of the Americas. They are small birds with long bills that help them extract nectar from flowers. Like the hummingbirds, many sunbirds (males particularly) exhibit brightly coloured plumage, with beautiful iridescent or “metallic” feathers that reflect the sunlight. In fact, the naturalist William Jardine tells us in his 1843 volume on the sunbirds that sunbirds get their name “from their brightly-tinted dress, appearing in higher splendour when played on by the sun-beams”. For hundreds of years, ornithologists have used the patterns and colours of these feathers to identify sunbird species. Now, however, we can combine multiple forms of data to uncover patterns that weren’t clear from plumage alone. Our paper also looked at the Black Sunbird (Leptocoma aspasia), a species with male plumage that’s hard to examine because it mostly looks jet-black, except when the sun hits it in the right way to reveal other colours. We found a genetic split in this species that had not been suggested by any previous work, probably due to its plumage being less informative.

Finding species like these isn’t just interesting for its own sake. It is also our best evidence to understand how evolution produces new species. This is particularly interesting in a region like Wallacea, which played such a significant role in the development of evolutionary biology. The observations that Wallace made around this region led him to discover evolution by natural selection, work which was published jointly with Charles Darwin in 1858 in the same journal where our sunbird paper has just appeared.

One of the observations that inspired Wallace’s evolutionary thinking was the importance of biogeographic barriers. Wallace noticed that the animals found on Sulawesi are markedly different from those on neighbouring Borneo, evidence that species would evolve on one island and then have difficulty crossing over. This boundary came to be known as Wallace’s Line. We now understand that it represents the beginning of the deep waters of the Wallacea region, which persisted even when sea levels were lower, unlike the shallower waters of the adjoining Sunda Shelf which gave rise to land bridges. A similar barrier to the east came to be known as Lydekker’s Line. As seen in the map below, the range of the Olive-backed Sunbird (in yellow) is currently thought to cross both Wallace’s Line and Lydekker’s Line, while the Black Sunbird (in purple) stops at Wallace’s Line but crosses Lydekker’s Line. It’s quite remarkable to imagine these dainty little birds maintaining gene flow across barriers which block so many other organisms! Our work, however, has indicated that the Olive-backed Sunbird populations on either side of Wallace’s Line actually represent separate species. The same is true of Black Sunbird populations divided by Lydekker’s Line. Modern evidence has actually reinforced Wallace’s original ideas, showing once again that these Lines represent significant biogeographic barriers that block gene flow in most animals.

Map showing populations sampled for our new paper. We found evidence that the Olive-backed Sunbird is actually composed of separate species in the Philippines (“Garden Sunbird”). the Sunda Shelf (“Ornate Sunbird”), the Wakatobi Islands (“Wakatobi Sunbird”), and the islands from Sulawesi to the Sahul Shelf (“Sahul Sunbird”). We also found that Black Sunbirds in New Guinea are strongly genetically divergent from those in Sulawesi. These findings reinforce the importance of biogeographic barriers like Wallace’s Line and Lydekker’s Line to evolution.

Both evolutionary biologists and ecologists are gaining new insights from large datasets on the traits and genomics of species. However, as these datasets are organised by species, they rely on our species lists being accurate in the first place. Data from  “species” like the Olive-backed Sunbird or Black Sunbird might prove misleading, as each of these actually represent multiple species. Meanwhile, a small population like that of the Wakatobi Sunbird may not be included in such a dataset at all if it isn’t recognised as a species.

To quote an 1863 paper by Wallace, the world’s species represent “the individual letters which go to make up one of the volumes of our earth’s history and, as a few lost letters may make a sentence unintelligible, so the extinction of the numerous forms of life which the progress of cultivation invariably entails will necessarily render obscure this invaluable record of the past”. It is therefore an irrevocable loss to the world, to humanity, and to science when a species goes extinct while still unrecognised, “uncared for and unknown”.

Hoga, one of the Wakatobi Islands where sunbirds were sampled for this study. It has been a privilege to see such beautiful places and animals for this research.

While the Wakatobi Islands are biogeographically “remote” due to their small size and the permanent water barriers that surround them, it is worth noting that they are not the stereotypical “desert islands” Western readers may imagine. The islands have been part of important shipping lanes since at least the 14th century, and the people of the Wakatobi are known for their maritime traditions and unique language. As Dr David Kelly, the second author on the recent paper remarked: “The identification of the Wakatobi Sunbird serves to remind us that biodiversity is everywhere. This bird wasn’t found in a remote rainforest, but along the scrubby margins of busy towns and villages. Let us hope the children of the Wakatobi will be able to enjoy these special birds for generations to come.”

A relief from Borobudur Temple on Java, built over 1000 years ago. The birds in the yellow boxes were identified as Olive-backed Sunbirds by Ashari et al. (2021). Their fascinating paper is available at https://li01.tci-thaijo.org/index.php/tnh/article/view/253401

The beauty of the sunbirds has attracted scientists and artists for many years. Elsewhere in Indonesia, Java’s Borobudur (the largest Buddhist temple in the world, constructed in the 8th or 9th century CE) displays carvings of Olive-backed Sunbirds drinking nectar on its walls. The researchers who identified these carvings hypothesise that this symbolises the Buddhist ideal of enlightenment. Over a thousand years later, sunbirds are still enlightening us on the origin of species.

Female (top) and male (bottom) Olive-backed Sunbirds, from Shelley’s monograph, published 1876-1880 and available from the Biodiversity Heritage Library at https://doi.org/10.5962/bhl.title.53516. Our new paper has found that the Olive-backed Sunbird is actually made up of at least four separate species.

To find out more, read our paper in the Zoological Journal of the Linnean Society here: https://doi.org/10.1093/zoolinnean/zlac081

Tramps in Transition: Wallacea’s monarch flycatchers and their evolutionary natural experiment

Pale-blue Monarch on the left and Island Monarch on the right

A warm welcome back to all our readers! The new year is now well and truly upon us and we hope you’ve all had a safe and energised return to work. This blog is written by Fionn Ó Marcaigh, summarising his new paper. Congratulations Fionn and we hope our readers enjoy learning about your research as much as we have! So without further ado…

Science is about making observations from the natural world, drawing up hypotheses to explain the patterns you’ve observed, and then testing these hypotheses by experimentation. We tend to imagine scientists in white coats doing experiments in the lab, but our understanding of evolution also owes a lot to work done in “natural laboratories” like islands and other isolated habitats, where evolution has taken place under different conditions. Our new paper, just published Open Access by the International Biogeography Society in their journal Frontiers of Biogeography, has used an important natural laboratory in Southeast Asia to test a classic hypothesis based on a bird called the Island Monarch (Monarcha cinerascens). We’ve made observations that contradict parts of the hypothesis and discovered a possible new species in the process!

Our natural laboratory was a collection of islands around a region known as Wallacea in central Indonesia (see map below). Named after Alfred Russel Wallace, this is where he co-discovered evolution by natural selection while travelling around islands of all shapes and sizes, with the waters around them being so wide and deep that most species have trouble crossing them. Some organisms are better at crossing these barriers than others, with the Island Monarch thought to be particularly adept. As its name suggests, the Island Monarch is one of the kings of small islands. It can be found all the way from the islands off Sulawesi in Wallacea, to the farthest reaches of the Melanesian islands east of Papua New Guinea, but is missing from large islands like Sulawesi and New Guinea themselves.

Continue reading “Tramps in Transition: Wallacea’s monarch flycatchers and their evolutionary natural experiment”

Evolution in the understorey

Sulawesi babblers from several islands

What is the first image that comes to mind when you think of evolution? Possibly a line of cartoon primates marching, slouching monkeys at one end and naked men with spears at the other. Or a branching tree diagram where each twig represents an organism, maybe with a tentative “I think” scribbled above it. Alternatively, you may have pictured an illustration of related birds from isolated islands, each showing a dramatically different bill shape adapted to a different diet. Darwin’s Galápagos finches represent a foundational influence in terms of where we tend to look for signs of evolution and what we expect these signs to look like. Our new paper, just published Open Access in Zoologischer Anzeiger: A Journal of Comparative Zoology, provides a contrasting image. We looked at the Sulawesi babbler (Pellorneum celebense), a dull brown bird that spends its time hiding in bushes on less isolated islands in Indonesia, looking pretty similar from one island to the next. Nevertheless, we found that several of its populations are quite different from one another in mitochondrial DNA, in morphology, and in song.

Continue reading “Evolution in the understorey”

Two new bird species from the unique and understudied Sulawesi region

This blog was first published on #theBOUblog. Check it out at https://www.bou.org.uk/blog-oconnell-two-new-white-eye-species-sulawesi/

The Wallacea region has always been known to be home to many unique species, with birds of paradise, giant reptiles and marsupial versions of sloths found among its many islands! The region takes its name from Alfred Russel Wallace, who along with Darwin, developed the theory of evolution from his studies of the species of Wallacea. When I first set my heart on a career as a Zoologist (a decision made with absolute certainty at age 12!) I dreamed of following in the footsteps of these great naturalists. So it is of no surprise that when I finally got around to starting my PhD many years later, I chose to study speciation (the formation of new species during the course of evolution) in the birds of Wallacea, with the hope the region still held mysteries to uncover. Our research focused on South-east Sulawesi, Indonesia. Sulawesi is a weird and wonderful part of the world, and island hopping through that region has provided me with a lifetime of unforgettable memories. It also allowed me to fulfill my dream, as in our recent paper in the Zoological Journal of the Linnean Society, we describe two new bird species from the Wakatobi Islands, an island chain off South-east Sulawesi (Figure 1).

Continue reading “Two new bird species from the unique and understudied Sulawesi region”

Kingfisher Evolution in the Wallacea Region

Studying diversification in the Todiramphus kingfishers of Sulawesi often brought to mind the adage, ‘what is rare is beautiful’. Though I certainly also learned that rare beauties can be incredibly frustrating! While I could be guaranteed to catch my other main study taxa, Zosterops white-eyes, by the dozen in the right habitat, Collared Kingfishers (Todiramphus chloris) and Sacred Kingfishers (Todiramphus sanctus) were much more elusive. This made them maddening study species, but ensured that every time I got to grips with one was a special moment. Each bird caught was measured and had a few flank feathers taken before release. Even the most disappointing site could be made worthwhile by catching a kingfisher. In particular, I’ll never forget a particularly fetid swamp in the backwoods of Sulawesi, as I’m pretty sure all the mosquitos in the world lived there. It yielded our worst ever bird catches, but two crucial Collared Kingfishers! These moments of elation have stuck with me, and have ensured that the Todiramphus kingfishers are the study species I’m most fond of.

Darren O’Connell and Adi Karya examine birds, while being examined by passers-by. Photo by Suliman La Ode.

Continue reading “Kingfisher Evolution in the Wallacea Region”

The Wakatobi Flowerpecker: the reclassification of a bird species and why it matters

Wakatobi Flowerpecker - Male

I posted previously about my PhD research studying bird populations from the tropical and biodiversity-rich region of Sulawesi, Indonesia. I am happy to announce that the first paper as part of this research has just been published in the open access journal PLOS ONE. To read the full paper for free, click here. This work is a collaborative effort from staff in the Department of Zoology in Trinity College Dublin and Haluoleo University in Sulawesi. Here, I’d like to discuss the wider importance of the findings of this study.

My current research focuses on bird populations from peninsular South-east Sulawesi and the nearby Wakatobi Islands. The main focus of this paper was to reassess the taxonomic status of a population of birds from the Wakatobi Islands (i.e. whether these birds represent a species or subspecies). The birds in question belong to the flowerpecker family (Dicaeidae); a group of small and colourful, arboreal passerines found from Southeast Asia to Australia. The Wakatobi birds were originally described as a separate species (Dicaeum kuehni) from those on mainland Sulawesi by the renowned avian taxonomist Ernst J. Hartert. However, for reasons that remain unclear in the literature, the Wakatobi birds were later reclassified as a subspecies of the Grey-sided Flowerpecker (Dicaeum celebicum) from mainland Sulawesi. Therefore we decided the Wakatobi populations were deserving of reassessment. From comparisons of plumage and morphology (that is, the measurement of various features such as a bird’s wing and bill), as well as estimates of genetic divergence and phylogenetic relationships between Wakatobi and Sulawesi populations, our results suggest the Wakatobi birds deserve to be recognised as a distinct species. We have therefore recommended the Wakatobi populations be reclassified as Dicaeum kuehni, a species found only on the Wakatobi archipelago and put forward the common name ‘Wakatobi Flowerpecker’.  For more detailed methods and results check out the paper.

“So what?”, you might say. Well, despite centuries of work from naturalists aiming to estimate the number of different species that exist or have existed on Earth (be they animal, plant, fungus, bacteria, etc) and further understand their evolutionary relationships, we still have a lot to learn! Therefore, this research adds another tiny piece to this enormous and incomplete jigsaw. Through a greater understanding of life on Earth we can attempt to answer some of the great philosophical questions, such as ‘Where and how did life start?’; ‘How and why do new species appear?’;  ‘Why has life evolved to become as it is today?’; and ‘How have we, as humans, come to be?’. Anyway, let’s be honest, who doesn’t enjoy learning of a recently discovered species or simply one they haven’t heard of before (be they as cute as the recently discovered olinguito or as frighteningly ugly as the goblin shark)? But the endeavour to discover species and classify and quantify the diversity on life on Earth brings us much more than entertainment and endless fascination, it also has very practical applications. Data on the distribution and conservation status of species are one of the major sources of information used to inform conservation policy. Therefore, as we are in the midst of an extinction crisis, it is vital that these data are accurate.

In order to maximise our understanding biodiversity, particularly in the remote and poorly known Sulawesi region of Indonesia, we require multi-disciplinary research. For example, take a look at Figure 1 below. On the left are a male (above) and a female (below) Grey-sided Flowerpecker from mainland Sulawesi. On the right are a male (above) and a female (below) Wakatobi Flowerpecker. They look very similar, right? This is true. However there are subtle but consistent differences in plumage between the species (again, see the paper for more info on this). Without the collection of detailed morphological data and the generation of genetic sequences, we may have incorrectly concluded that these make up just one species, when in fact they are morphologically distinct, reproductively isolated and genetically very different. This demonstrates the need for modern research, not just in Sulawesi, but globally, to employ integrative research, combining traditional comparisons of colour, size and shape with modern genetic and phylogenetic analyses.

Figure 1. Plumage comparisons-p18pjcggcs1dgo1ulm1sor9s214bc
Figure 1. A comparison of plumage characteristics between male (top row) and female (bottom row) Grey-sided Flowerpeckers (left) and Wakatobi Flowerpeckers (right).

Despite the knowledge that the Sulawesi region is home to a large number of remarkable birds that are found nowhere else in the world, it has remained relatively poorly studied. Furthermore, there has been a lack of integrative ornithological research in the area and very little genetic sampling. Therefore, it is likely that avian species richness for the Sulawesi region is underestimated and that numerous bird species are awaiting description. On top of this, Sulawesi’s biodiversity is facing major threats from a rapidly expanding human population and mass habitat destruction, among other things. Unless we can encourage more multi-disciplinary research within the region, we will likely fail to recognise evolutionarily distinct lineages and run the risk of losing them forever.

Our current findings inspire many further questions. For example, why have the flowerpeckers on the Wakatobi islands become so different to their close relatives on mainland Sulawesi? In other words, what are the evolutionary pressures that have driven the divergence of the Wakatobi Flowerpeckers? By investigating these questions, we hope to learn more about the evolutionary processes of speciation and adaptation to living on islands. As the Wakatobi Flowerpecker is found only on the Wakatobi Islands, the protection status afforded to the islands may require reassessment. Furthermore, considering one unique bird species has evolved on the Wakatobi, could there be more? Watch this space.

Author and Images:  Seán Kelly, kellys17[at]tcd.ie, @seankelly999

Seminar series: Tom Ezard, University of Southampton

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Part of our series of posts by final-year undergraduate students for their Research Comprehension module. Students write blogs inspired by guest lecturers in our Evolutionary Biology and Ecology seminar series in the School of Natural Sciences.

This week; views from Sarah Byrne and Sean Meehan on Tom Ezard’s seminar, Birth, death and macroevolutionary consequences.

Splitting Hares – easier said than done?

In a recent talk given by Tom Ezard, a research fellow and evolutionary ecologist, the definition of a species was examined and challenged. While defining a species may seem a simple task for just about anybody and in particular a room full of people with a biology background, the actual definition can be harder to understand when thinking about fossil or species’ records and gaps across time. Ezard highlights that a dynamic approach is needed when discussing speciation and the definition of a species. Claiming that you shouldn’t define a species at one particular moment in time, he details that large gaps in the fossil record make it very difficult to have a fully complete picture about speciation events. In other words, making inferences about speciation events from a certain snapshot in time could overlook the dynamic process of change that occurs over time and give us inaccurate theories about the macroevolution of species.

Following on from the definition of a species, Ezard was interested in the fossil record and how it can give us information about the species record and also, more importantly, about diversity. He was interested in finding out where these gaps in the fossil record had occurred and what impacts they could possibly have. In graphs he provided, it was clear that there was a difference between data over time with more species surges found in recent data in comparison with the past, indicating the number of species has increased over time. However, it’s a little misleading because as time develops we learn more about how to indentify species of have better techniques to do so, it is therefore unclear as to whether or not there has been a big increase in species.

To better explain some complicated parts of the speciation theory, Ezard used a baseball analogy which I was thankful for, showing a picture of various baseballs over time. Ezard explained how techniques improve over time and how the original was very different to the new and modern ball. All of the baseballs of various different ages, textures and shapes remained part of one game (or one species) and that there was no split into a new game (or new species). He stressed that this continuation was very important in understanding macroevolution and when identifying species, that it was vital to look at gaps in the lineage. This brings us back to the fact that the fossil record needs to be examined further and the question of what is meant by a species may need to be redefined. Ezards definition of a species as ‘a single line of descent, a sequence of populations evolving separately from others seems closer to the real definition than previously thought.

Speciation was also a key factor of Ezard’s talk and he was interested in identifying budding speciation events while still being able to identify their ancestors. Two main types of speciation and evolution were discussed in the talk, one type; anagenesis refers to a change along a branch of a phylogeny or the evolution of a gradual change within a species over time. This theory was backed by Darwin and eventually leads to a speciation event. In contrast, cladogenesis, where a population stays stable until a big speciation event happens suddenly and then a splitting occurs between species that ensures they can then not reproduce with each other.

The split can be caused by either biotic or abiotic factors with disagreements regularly occurring between geologists and modern evolutionary biologists over whether the biotic factors (such as competition) or the abiotic factors (such as climate) are the main key drivers affecting species ecology and diversification. So, what is the main driver affecting species ecology and in turn speciation and diversification? Ezard was interested in finding this out.

Using observational studies, algorithmic processes and a multivariate complex approach, Ezard was able to account for ecological differences between species. Lotka’s equation gave an estimate of birth and death models that detailed speciation probability and extinction risk. Species respond differently to global drivers of change and these differences have macroevolutionary consequences. The Red Queen Hypothesis mentioned above, a biotic factor that describes how predator and prey are continually adapting to out-do each other affects species much more so than climate does, and in comparison, climate, an abiotic factor has much more of an effect on extinction.

So, it seems that a combination of both factors are important although they affect both speciation and extinction at different rates. Ezard indicated that, in order to understand diversity, it was first necessary to understand the biotic factors that impact the split and to then devise a model to draw these two areas together. Ezard’s enthusiastic and engaging approach clearly showed his passion for the subject and the interesting topic left me with a lot to think about it.

Author: Sarah Byrne

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Lumpers and Splitters: Apparently they’re not varieties of potato

What is a species? This question seems so fundamental to biology that surely the experts have answered it by now, right? Wrong. Defining a species is a difficult thing, and each new definition seems to come up short in certain criteria. For example Ernst Mayr’s widely used definition of a species: “groups of actually or potentially interbreeding natural populations, which are reproductively isolated from other such groups” completely disregards species which reproduce asexually. For this reason I like Simpson’s evolutionary concept for defining a species and this is precisely what Tom Ezard uses for his work on macroevolutionary dynamics. This concept holds that each species represents a single line of descent; it begins with a speciation event and terminates with extinction. Ezard used the evolution of the baseball to demonstrate this concept. Although the modern baseball is considerably different from its original ancestor, it is still a baseball and there have been no ‘speciation’ events or splits in the lineage to form a new type of ball.

It was Darwin who first coined the term ‘lumpers and splitters’. Lumpers are those biologists who tend to ‘lump’ many ‘species’ in together as one. The splitters are those biologists who like to make as many ‘species’ as possible. In his 1945 work ‘The Principles of Classification and a Classification of Mammals’ George G. Simpson notes rather sardonically: “splitters make very small units – their critics say that if they can tell two animals apart, they place them in different genera … and if they cannot tell them apart, they place them in different species. … Lumpers make large units – their critics say that if a carnivore is neither a dog nor a bear, they call it a cat.” So we can see that this problem is an old one, and that Simpson’s evolutionary concept is very useful for defining species in macroevolutionary studies.

In order to study macroevolutionary dynamics one needs a fairly detailed picture of a clade’s development, and not many organisms provide a suitable fossil record for a detailed study. Fortunately Ezard and his team found the perfect organisms for this purpose; the Foraminifera. These creatures are marine dwelling amoeboid protists. When they die they sink to the bottom and leave behind their calcium shells or tests. They are deposited and preserved on the sea floor and in the right conditions over time can form stratified layers of fossils which give a very complete picture of their evolution over time. Also,the stable isotope ratios of oxygen in the shells can be used to reconstruct palaeo-climatic conditions. These attributes make them incredibly useful in the study of macroevolutionary dynamics.

So, what are the driving forces of speciation? Is there one factor which influences this process above all the others? This is what Ezard and his team set out to investigate. The foraminifera had an interesting story to tell. It was found that incipient species diversify the fastest. This was found to be primarily due to biotic factors or ‘Red Queen’ factors. As a clade grows older it was found that diversification slows due to diversity dependence. However, it was found that extinction is primarily influenced by climatic or Court Jester factors. These findings are important in order to grasp a general understanding of macroevolutionary dynamics. It means that impacts of diversity and climatic fluctuations are not felt uniformly across a phylogeny.  More simply put, it means that the extent of the effect of biotic and abiotic factors on a clade depend on how old it is.

In summary, what Ezard and his team found was that there is no dominant macroevolutionary force, but that, a combination of biotic and abiotic variables drive speciation and extinction. They also found that species’ ecologies are important driving forces in these processes.

Author: Sean Meehan

Image Source: Wikicommons