Why are there so many more species in some regions than in others? According to a recent study, competition for ecological niches limits the evolution of new species. Further, this study, which analysed the genetic and evolutionary relationships between all 461 species of Himalayan songbirds, found that the rate of speciation slows or even stops as available ecological niches fill up.

NOTE: can't see any pictures? This story is best viewed in "classic".

The world's "hottest" hotspot for songbird species diversity

The songbirds (oscines) suborder of passerines is a wildly successful evolutionary story. Many of the most common and familiar wild birds -- sparrows, finches, thrushes, warblers, larks and swallows -- are oscines. Grouped together based on the strong structural similarities of their vocal organ, the syrinx, members of this taxonomic suborder are surprisingly diverse, featuring tremendous variations in body mass, shape and feeding adaptations, and inhabiting all terrestrial habitats.

Despite their morphological and ecological diversity, songbirds arose from just a single ancestral species that appeared approximately 50 million years ago near modern day New Guinea (doi:10.5122/cbirds.2013.0014). Around 34 million years ago, Earth's rapidly cooling climate triggered the oscines to expand into Asia where they quickly diversified to exploit the many ecological niches that they found there.

Like all groups of living beings, avian taxonomic groups are patchily distributed, their global distribution depending more or less upon biogeographic accident. For example, although more bird species live in South America than anywhere else, Asia is where the songbirds achieved their greatest diversity.

"South America was an island for a long time", said Trevor Price, lead author on this new songbird study and a Professor of Biology who studies avian speciation at the University of Chicago.

According to Professor Price, this geographic isolation prevented oscines from colonizing South America until recently: following a circuitous route, songbirds spread through Asia and into North America before finally arriving in South America just 15 million years ago.

Today, there are roughly 5000 oscine species, comprising almost half of all modern bird species, many of which began differentiating within the first 10-12 million years of their explosive climate-triggered radiation. Currently, there are nearly as many songbird species as there are mammalian species.

Within Asia, the Himalayas are home to more than 460 songbird species (Figure 1b; larger view) that are found nowhere else, with more than 360 of those species occurring in a narrow band stretching from eastern Nepal through China, India, and Myanmar (Figure 1a; larger view):

How and why did this unique species-rich songbird community pop up in the eastern Himalayas? Which then leads to the general question: why do some regions have more species than others? The answer to this simple question is surprisingly complex, and has mystified scientists and naturalists for centuries.

A scientific paper was recently published that explores this question by combining decades of field surveys, DNA analyses and other research conducted by an international team of experts from India, the USA, Germany, and Sweden. Co-led by Professor Price and Dhananjai Mohan, the Chief Conservator of Forest with the Indian Forest Service, this team focused their research efforts on a 10,000 km2 region located in the states of Bengal, Sikkim and Arunachal Pradesh (the boxed-in area on the map in Figure 1a; larger view). This area, which is this research team's field site, is home to 358 songbird species, making it the "hottest" hot spot on Earth for songbird biodiversity. The number of species living in this area is beyond compare: as any knowledgeable birder can tell you, you'd be lucky to find 100 songbird species in a similarly-sized area in either North America or Europe.

Further, the Himalayas are mostly unexplored, so scientists are still discovering new songbird species there. Most of these newly discovered species occupy very small ranges, have small populations and are found nowhere else in the world.

One such recent discovery is the Bugun liocichla, Liocichla bugunorum (above). This small songbird was first spotted just 10 years ago by Ramana Athreya of the Indian Institute of Science Education and Research in Pune, and the bird is still known only from a handful of pairs breeding in a tiny area at the edge of the Eaglenest Wildlife Sanctuary in Arunachal Pradesh. Although new to science, this bird represents a discrete species: DNA isolated from a feather revealed this species diverged more than three million years ago from its closest known relative, which lives in the mountains of central China.

Speciation and geography: are they related?

Most new species are thought to arise in a three step process: First, a species expands its range. Then a barrier, such as a geographic event, separates the species into distinct populations. Last, development of the inability to interbreed -- reproductive isolation -- finalizes the speciation process. As this cycle repeats, it gives rise to a vast diversity of plant and animal species.

Currently, scientists are testing several hypotheses, or potential explanations, for why some geographic regions have larger clusters of species than others. Since more than one of these hypotheses may be germane to any one location, time period or taxonomic group, unraveling this complicated natural process is challenging. The hypotheses that are being tested include;

the time it takes for speciation to occur. One hypothesis suggests that species-rich areas, such as the tropics, are ancient and have remained relatively unchanged for long periods of time, thus allowing speciation to occur with few disruptions. This contrasts with younger and more heavily disturbed regions, particularly the temperate zone, where there is less biodiversity.

the rate at which species appear or go extinct. These hypotheses propose that ancient pristine areas, such as the tropics, may either function as a "museum" -- where the extinction rate is low -- or as a "cradle" -- where speciation rate is high -- particularly compared to temperate zones.

the geographic differences in number and variety of niches that can accommodate new species. Simply stated, this hypothesis suggests that some geographic regions have a greater abundance or diversity of resources than others, which in turn, accommodates the formation of more species.

In this study, Professor Price, Dr Mohan and their colleagues used several approaches to examine how geographic differences affect speciation by testing the niche-filling model: first, they asked whether the geography of the eastern Himalayas provided a greater number and diversity of niches that songbirds could occupy and adapt to. Second, they examined whether the rate of oscine speciation changed over time. Third, they investigated the diversity and abundance of resources available in different ecological niches.

Does Himalayan geography support songbird speciation?

Previous studies in leaf warblers (doi:10.1038/355817a0) and in the corvoidea (doi:10.1111/j.1558-5646.2012.01618.x) found that closely-related bird species apparently colonise ranges at different elevations after differences in feeding method and body size have appeared. But is this pattern true for other songbirds? Specifically, might the entire eastern Himalayan songbird assemblage have followed this evolutionary pattern?

To answer this question, Professor Price's and Dr Mohan's team turned to their extensive phylogenic tree for eastern Himalayan birds (Figure 1b; larger view). Reconstructed from DNA samples collected from all 461 songbirds and other bird species living in the Himalayas, this is the largest and most complete regional avian DNA database compiled so far. The dating for this phylogeny was calibrated using multiple bird fossils collected elsewhere in the world so it is accurate to within three million years.

Previous work with this phylogeny indicates that, on average, each east Himalayan songbird species has been separated from its next closest relative in the region for 6-7 million years (doi:10.1098/rsbl.2013.1067). This is roughly about the same length of time that humans and their closest relative, the chimpanzee, have been separated.

To better understand the birds' adaptations to their habitats, the team weighed songbirds and measured the length of their tarsus (lower leg bone) and beak using museum specimens. These morphological traits were then analysed within the context of the birds' evolutionary relationships.

The team estimated the number of oscine lineages for any given "time slice" through their dated phylogeny (blue line; figure 2a; larger view) and compared this to disparity measures for the three morphological traits measured in the field. Disparity measures plot the total physical variance within the clades spanned by any given "time slice" (mass = solid black line; beak and tarsus length = dashed black lines. This paper -- doi:10.1126/science.1084786 -- is especially enlightening about disparity plots.):

Several patterns emerged: first, starting with just a few, very distinct, lineages, new species initially appear very rapidly but this rate of speciation declined precipitously over time as more species appeared and colonised more ecological niches.

"Despite the great diversity of environments and ability for species to move between areas, evolution in the eastern Himalayas appears to have slowed to a basic halt," said Professor Price.

"Other species have formed elsewhere, such as in China and Siberia, but most have been unable to spread into this region."

Second, the Himalayan songbird assemblage showed numerous morphological differences in feeding method and body size early in their evolutionary history. For example, when the research team evaluated the rate of morphological change within six songbird lineages dating back to 11.5 million years ago (represented by one species from each lineage from top left; Phylloscopus xanthoschistos, Parus monticolus, Acridotheres fuscus, Dicrurus paradiseus, Carpodacus rubicilla and Leucosticte brandti in Figure 2b, larger view), they found that songbirds with longer legs tended to develop smaller beaks, whilst those with shorter legs tended to evolve larger beaks.

Perhaps the most striking finding is that closely-related species often occupy different elevational zones, indicating that elevation is the last niche dimension along which they diverged. That discovery is illustrated below for three species of sunbirds (two other close relatives are not shown; larger view):

Further, the researchers noted that newer species' ranges decreased in size.

"Our argument is that niche filling has stopped [younger] species from getting big ranges," said Professor Price.

"In the eastern Himalayas, it has become harder and harder for new species to get into that system, and we are quite close to the maximum number of species that can be accommodated. There is little room for more species because niches are increasingly occupied."

These findings suggest that speciation and geography are intimately connected in the evolutionary history of the Himalayan songbird assemblage: initially, numerous morphological differences in feeding method and body size appear early in their evolutionary history, whereas only later did the fledgling species invade and adapt to available ecological niches at different elevations. Since available niches were filling up as new species moved in, younger and younger songbird species were usually competing for smaller and smaller niches. These findings are all consistent with the niche-filling model.

Speciation and elevation: are they related?

When Professor Price and his team examined the phylogenetic relationships between closely-related songbirds living at different elevations, they found that, as elevation increased, phylogenetic relationships decreased, indicating higher elevation birds speciated more recently (figure 3a; larger view):

Using songbird morphological diversity as a proxy measure for niche resource diversity, Professor Price, Dr Mohan and their colleagues tested whether the variation of resources available in particular niches might explain the observed songbird species distribution patterns throughout the Himalayas (Figure 3b; larger view). They found that despite their closer relationships, songbird morphological diversity increases along an elevational gradient -- even up to the highest elevations, despite there being fewer species living at these elevations.

"One of the neatest results is that the songbird community is more morphologically diverse at high elevations than at low elevations, apparently because it comprises a larger portion of the overall avifauna at high elevations, hence it occupies a broader range of niches", said Christopher Witt, Associate Professor of Biology at the University of New Mexico, who was not involved with this study.

"The varied communities at different elevations are highly distinct from ecological, morphological, and phylogenetic perspectives, and these communities are interdigitated along the [elevational] gradient", said Professor Witt in email.

"This is true even though the phylogenetic diversity of species in those high elevation communities is lower than it is at low elevations", said Professor Witt in email.

The research team thinks these characteristics are probably due to two factors; a lack of competition from other non-passerine bird species, which predominate at lower elevations (Figure 1c, larger view), and the presence of available niches at higher elevations.

Why are Himalayan songbird species most abundant at 1800m?

If you looked carefully at figure 1c (larger view), you noticed there are more oscine species at 1800 metres elevation than anywhere else. This is contrary to most peoples' expectations that biodiversity is greatest in lowland rainforests.

On the other hand, most people probably don't know that the eastern Himalayan rainforests are rather lush at this elevation -- quite unlike what most people imagine as a montane rainforest. But nevertheless, this raises the question: why are there more songbird species at mid-elevations than, say, in the Himalayan lowland rainforests?

On closer inspection, Professor Price's and Dr Mohan's team found that there is a very good reason for this peak oscine abundance at 1800 metres (figure 4a; larger view) -- food: this is where insects and other arthropods are most abundant (figure 4b; larger view):

Despite the lower mid-elevation rainfall and temperatures, annual winter freezes trigger an annual springtime leaf and arthropod explosion -- a veritable food bonanza for insectivorous songbirds, especially when compared to lowland rainforest. Further, the lowlands are occupied by a plethora of insectivorous animals that probably compete effectively with songbirds for this particular food resource. These animal competitors include nonpasserine and suboscine birds (Figure 1b; larger view).

But the most important factor may be ... ants: the insectivorous weaver ant species, Oecophylla smaragdina, is abundant at low elevations but absent from mid-elevations where songbird diversity is greatest. Thus there is a greater abundance or diversity of food resources available that are not exploited by ants, and this in turn, supports a greater diversity of songbird species.

Does this study conflict with that hummingbird study that I shared?

Does this study's findings conflict with that faboo hummingbird study that I shared a few months ago? In a word, no.

To recap, the hummingbird study found that the rising Andes are tightly linked to the rapid speciation of hummingbirds -- a process that is still happening at a rapid rate. Although Professors McGuire's and Witt's team are investigating other research questions about the physiology of hummingbirds, the fundamental issues they address about hummingbirds' patterns of speciation overlap remarkably well with Professor Price's and Dr Mohan's findings for Himalayan songbirds. Since mountainous uplift presents a wealth of new niches and micro-habitats that offer new opportunities for speciation to occur, the consistency between the hummingbird study and the Himalayan songbird study shows that the speciation process for two unrelated groups of birds living on different continents are strikingly similar.

Where next?

"To me, the most interesting thing is our main conclusion that niche filling might limit the rate of speciation", said Per Alström, a co-author on the paper. Dr Alström is a molecular taxonomist based at the Swedish University of Agricultural Sciences where he studies the systematics and evolution of Asian birds.

"Moreover, I'm thrilled about the finding that the peak in number of bird species at around 1800 metres is mainly caused by species feeding on insects and that also the insects are most abundant at that elevation", said Dr Alström in email.

But many questions remain unanswered about how niche-filling affects the speciation process.

"However, I must admit that I find it a bit puzzling that niches can become that full, except for species with highly specialised requirements that are scarce", Dr Alström added. "Hopefully, our study will stimulate further research in this field."

But this research also highlights very real conservation concerns.

"I think this paper will help bring more attention to the importance of protecting habitat corridors along elevational gradients that clearly expand species diversity by lifting the limits on the number of available niches", said Professor Witt in email.

Although the Himalayan songbirds are survivors, they may have finally met their match in human-caused global warming and habitat destruction.



"It's important to realize just how old and how much incredible genetic diversity are in these mountainous forests," said Professor Price.

"All these species managed to deal with warming, glaciation and cooling without changing very much. It's quite amazing to me to think that in the next 100 years a lot of these may be gone, when they managed to get through the last 6 million years."

Sources:

Price T.D., Hooper D.M., Buchanan C.D., Johansson U.S., Tietze D.T., Alström P., Olsson U., Ghosh-Harihar M., Ishtiaq F. & Gupta S.K., Martens J., Harr B., Singh P. & Mohan D. (2014). Niche filling slows the diversification of Himalayan songbirds, Nature, 509, 222–225. doi:10.1038/nature13272 [$]

University of Chicago press release.

Trevor Price [email; 15 April 2014]

Per Alström [emails; 6, 13, 14 May 2014]

Christopher Witt [emails; 6 May 2014]

Bob O'Hara [real-life discussion]

What's old is new again: newly discovered songbird family is ancient. (Discusses Alström & Price's newly discovered family of Himalayan songbirds -- comprised of just one species.)

Hummingbirds: still evolving endless forms most wonderful. (Discusses McGuire & Witt's paper, about the relationship between the Andean uplift and speciation in hummingbirds.)

Also cited:

Fjeldså J. (2013). Review: The global diversification of songbirds (Oscines) and the build-up of the Sino-Himalayan diversity hotspot, Chinese Birds, 4 (2) 132-143. doi:10.5122/cbirds.2013.0014 [OA]

Richman A.D. & Price T. (1992). Evolution of ecological differences in the Old World leaf warblers, Nature, 355 817-821. doi:10.1038/355817a0 [$]

Kennedy J.D., Weir J.T., Hooper D.M., Tietze D.T., Martens J. & Price T.D. (2012). Ecological limits on diversification of the Himalayan core Corvoidea, Evolution, 66 (8) 2599-2613. doi:10.1111/j.1558-5646.2012.01618.x [Free PDF]

Alström P., Hooper D.M., Liu Y., Olsson U., Mohan D., Gelang M., Hung L.M., Zhao J., Lei F. & Price T.D. (2014). Discovery of a relict lineage and monotypic family of passerine birds, Biology Letters, 10 (3) doi:10.1098/rsbl.2013.1067 [$]

Harmon L.J., Schulte J.A., Larson A. & Losos J.B. (2003). Tempo and Mode of Evolutionary Radiation in Iguanian Lizards, Science, 301 (5635) 961-964. doi:10.1126/science.1084786 [OA]

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