"There is grandeur in this view of life, with its several powers, having been originally breathed into a few forms or into one; and that, whilst this planet has gone cycling on according to the fixed law of gravity, from so simple a beginning endless forms most beautiful and most wonderful have been, and are being, evolved." ~Charles Darwin, On The Origin of Species (1859)

A newly-published comprehensive family tree for hummingbirds traces the rapid and ongoing birth of new species throughout this modern family's 22-million-year history. The findings indicate that hummingbird diversification is driven primarily by two elements: by their exploitation of new niches created by the Andean uplift and expansion into new geographic regions, and by their unique relationship to flowering plants. Combined, these two elements support the large variety of distinct hummingbird species that live side-by-side in the same places. Further, although the rate of hummingbird speciation is slowing, this study finds that the evolution of new hummingbird species is still ongoing and is far from complete.

Most people think hummingbirds require hothouse-like conditions to live. But in fact, more than one-third of all hummingbird species live in the extreme environments found in the Andes. This raises a number of important issues, not the least of which is how such tiny birds survive such cold nights.

As if overcoming that challenge isn't remarkable enough, hummingbird flight is the most energetically demanding form of vertebrate locomotion, yet these birds can be seen buzzing around blossoms at high elevations where oxygen concentrations are so low that humans become faint and are left gasping for breath. How do hummingbirds do that? Not long ago, I shared a beautifully-executed study that found that high-altitude hummingbird species evolved special hemoglobins adapted to low-oxygen environments [doi:10.1073/pnas.1315456110].

Now this same team of researchers has published another paper that investigates whether the rising Andean Mountains played a role in hummingbirds' colonization of high-altitude habitats and if this tectonic event affected how rapidly they've diversified ("speciated").

This collaborative study was led by Jim McGuire, Associate Professor of Integrative Biology at the University of California at Berkeley, and Curator of Herpetology at the university's Museum of Vertebrate Zoology. Professor McGuire's special focus is investigating the historical biogeography of the frogs and lizards on the Indonesian island of Sulawesi.

From herps to hummingbirds

Hummingbirds, which are exclusively found in the New World, are a long way from Sulawesi's reptiles and frogs, so what aroused this new interest?



"[M]y interest in hummingbird research was initially inspired by the sort of hallway conversation that often leads researchers down unexpected pathways", explained Professor McGuire in email.

"[B]ut the hook for me was the opportunity to further explore my interests in the evolution of flight performance in a phylogenetic context. Once I got started, I realized that hummingbirds are a spectacular system for comparative biology because they are so diverse and are quite amenable to experimental study."

Some of those experiments were conducted -- on both avian and human subjects -- high in the Andes.

"Our expedition was relatively short (2 weeks, as opposed to my typical 8-10 week sorties to Indonesia) so time was of the essence. Thus, we went directly from sea level at Lima to our 4000 meter elevation field site in ... 6 hours, which is not nearly enough time to acclimate properly", writes Professor McGuire in email.

"The first two days at the site were surprisingly challenging for me because I was out of breath all of the time. It was sufficiently bad that I could not get through brushing my teeth without pausing periodically to huff and puff. And I walked my gear up the mountain to our field site in 20-foot intervals. After two days of this and a continuous throbbing headache, I turned the corner and was good for the rest of the stay."

Other team members weren't so lucky; at least one soon returned to lower elevations to recover his health.

Twenty-two million years of hummingbird diversification

This published study is part of a much larger research project that investigates how hummingbirds adapted to extreme environments. A critical foundation upon which this decade-long project is based is reconstructing a detailed phylogenetic tree for the hummingbird family that includes as many species as possible. So far, this phylogeny includes sequences from six chromosomal and mitochondrial genes from 284 of the 338 described species -- the most comprehensive yet for this family of birds.

"The study took a decade to complete in part because it took a long time to collect 6 genes worth of data for more than 450 individual hummingbirds", said Professor McGuire in email. "[A]nd we kept adding samples to the matrix as tissues became available for previously unsampled species."

The team statistically analysed the rate of change for the six gene sequences to reconstruct a time-calibrated phylogenetic tree (figure 1, larger view):

These data suggest that hummingbirds split away from their sister group (their closest relatives), the swifts and tree swifts, roughly 42 million years ago in Eurasia. This date corresponds well to the oldest known hummingbird fossils, discovered in southern Germany and estimated to be 30 million years old [doi:10.1126/science.1096856].

This phylogeny shows that the most recent common ancestor to all modern hummingbirds is estimated to have lived just 22.4 million years ago somewhere in South America. This is quite recent for this modern avian family, particularly in view of the large number of species that are alive today, revealing these birds experienced a rapid rate of diversification after they reached South America.

Rising Andes led to soaring hummingbird speciation rates

Since modern hummingbirds only occur in the Americas, how did they get from Eurasia to South America? Considering their intense energy demands, the researchers think they probably followed the Bering Land Bridge from Eurasia into North America before continuing to South America. Once there, these nectar-feeding birds settled in and exploited the many different habitats and nectar resources available to them, specialising and then diversifying rapidly (figure 2A; larger view) into nine main clades (or groups) containing hundreds of species. The birds then moved back into North America approximately 12 million years ago, and then invaded the Caribbean (at least five times!) about five million years ago:

The rate at which new species appeared varied between these bioregions (North versus South America, for example). However, during their 22-million year evolution, the rate at which new hummingbird species appeared in the Andes is very similar to the rate that new species appeared in non-Andean habitats (figure 2B), suggesting that mountain-building played an important role in their diversification. These findings are consistent with a number of other studies of the effects that Andean mountain-building had upon biodiversity [as reviewed in doi:10.1126/science.1194585].

Why are there so many Bee hummingbirds?

There are several proposed explanations for the tremendous amount of biodiversity present in South America. One hypothesis is that the tropics support a stable and unvarying environment that supports speciation. The other idea is that the uplifting Andes presented a variety of new microhabitats and niches where natural and sexual selection could act on small isolated populations to give rise to new species.

To gain a more precise understanding of the effects that the Andean uplift had upon evolution rates in each hummingbird clade, the researchers reconstructed a time-calibrated family tree and colour-coded the average rate of radiation for eight of the nine clades as well as for each of the species examined so far. (Recall that the Patagona Hummingbird Clade has only one species so it was not included in the clade diversification rate analysis.) They found that the rate of diversification for the entire hummingbird family varied tremendously between groups (figure 3; larger view):

Although the entire hummingbird family diversified rapidly, diversification was especially dramatic for the Bee Hummingbird Clade.

"The Bees have the highest rate of diversification -- well above the black line denoting the overall diversification rate for hummingbirds", writes Professor McGuire in email.

Interestingly, the Bee Hummingbird Clade is the youngest in the hummingbird family.

"The Bee Hummingbird Clade originated only about 5 million years ago but has rapidly diversified into ~35 species", Professor McGuire explained.

This is even more remarkable when one considers that the Bee hummingbird group didn't pop up in an empty ecosystem; instead, they radiated in the presence of the richest avifauna in the world -- and at a time when the other eight hummingbird clades were already well established. So why are there so many Bee hummingbirds? No one knows.

Professor McGuire added that although the Bees and certain other groups are still diversifying rapidly and will do so for a long time to come, the rate of diversification has slowed for all hummingbird clades -- particularly for the Brilliants and Coquettes, which diversified primarily in the Andes.

Although the authors did not address this question in this study, I think female choice is playing an important role in hummingbird diversification. This scenario looks similar to the explosive speciation seen in freshwater cichlid fishes endemic to the African great lakes [i. e.; doi:10.1098/rspb.1998.0520]. In that case, there are a number of contributing factors that support rapid diversification, such as small territory size and intense specialisation -- both elements also present in hummingbirds. But in cichlids and in hummingbirds, female choice appears to be the driving force behind the evolution of new species. Consider, for example, the wide variety of plumage colours (particularly iridescence) and ornaments possessed by male hummingbirds, whereas the females of at least some species are difficult to distinguish. This scenario suggests that females select mates that possess the most conspicuous traits, which is predicted by the good-genes mechanism or by a runaway selection process.

Endless forms most wonderful

"I find it particularly fascinating that hummingbirds are so young, yet so diverse", writes Professor McGuire.

"[T]his study shows that hummingbird diversification is even more complex and remarkable than I would have imagined", said Professor McGuire. For example, whilst all hummingbirds depend upon flower nectar to fuel their high metabolisms and demanding flight, coordinated changes in flower and bill shape have helped drive the formation of new species of both hummingbirds and plants.

"One of the really cool features of hummingbird evolution is that they all eat the same thing yet have diversified dramatically," said Professor McGuire. "It really is a big surprise that hummingbirds have divided the nectarivore niche so extensively."

Remarkably, as many as 25 hummingbird species live together in some places.

Further, the researchers estimate that, if undisturbed, hummingbirds would continue to diversify until they reached a speciation/extinction equilibrium of perhaps as many as 767 species -- twice the number of species that we see today.

"We are not close to being at the maximum number of hummingbird species," said Professor McGuire. "If humans weren't around, they would just continue on their merry way, evolving new species over time."

This new study has provided unexpected revelations and added detailed insights into the evolutionary history of this modern family of birds.

"Finally, I remain surprised by our finding that hummingbird evolutionary history is incongruent with the traditionally recognized hummingbird subfamilies", said Professor McGuire.

"The traditional view is that hermit hummingbirds (Phaethornithinae) are the sister taxon of all other hummingbirds, which together compose the Trochilinae (or 'typical' hummingbirds)," explained Professor McGuire. "This view of the phylogeny of hummingbirds was consistent with a tidy story in which the drably colored, non-territorial hermit hummingbirds represented an evolutionary step leading to the appearance of territorial, vibrantly colored species with iridescent gorgets, etc."

But according to these new findings, hermit hummingbirds' closest relatives are topaz hummingbirds.

"[T]opazes are themselves vividly colored and their placement in our study as the sister taxon of hermits is inconsistent with the theory that hermits represent the primitive (plesiomorphic) state for hummingbirds", explained Professor McGuire.

Other findings:

the Marvelous Spatule-tail, Lodiggesia mirabilis, is nested deeply within the Puffleg (Eriocnemis) clade

all eight Emerald hummingbirds genera (comprising more than a few species) are paraphyletic

"One thing is clear, hummingbird taxonomy is going to require substantial modification as a result of our study."

But this exciting study is just part of a much larger body of research.

"The big phylogeny is really just phase one", said Professor McGuire. "[W]e have some really cool ongoing work on hummingbird adaptation to low-oxygen (hypoxic), high-elevation environments that will follow."

Sources:

McGuire J.A., Witt C.C., Remsen, Jr. J.V., Corl A., Rabosky D.L., Altshuler D.L. & Dudley R. (2014). Molecular Phylogenetics and the Diversification of Hummingbirds, Current Biology, doi:10.1016/j.cub.2014.03.016

Jim McGuire, emails [1-4 & 7 April 2014]

Press release

Many thanks to Jim McGuire for his long explanations and for digging up additional images so I could share them with you. Also, many thanks to a twitter pal, @dandavishello, for sending me a requested PDF on a sunny Sunday morning.

Also mentioned (and worth reading):

Hoorn C., Wesselingh F.P., ter Steege H., Bermudez M.A., Mora A., Sevink J., Sanmartin I., Sanchez-Meseguer A., Anderson C.L. & Figueiredo J.P., C. Jaramillo, C., Riff D., Negri F. R., Hooghiemstra H., Lundberg J., Stadler T., Särkinen T. & A. Antonelli. (2010). Amazonia Through Time: Andean Uplift, Climate Change, Landscape Evolution, and Biodiversity, Science, 330 (6006) 927-931. doi:10.1126/science.1194585 [free PDF]

Mayr G. (2004). Old World Fossil Record of Modern-Type Hummingbirds, Science, 304 (5672) 861-864. doi:10.1126/science.1096856 (OA)

Doorn G.S.V., Noest A.J. & Hogeweg P. (1998). Sympatric speciation and extinction driven by environment dependent sexual selection, Proceedings of the Royal Society B: Biological Sciences, 265 (1408) 1915-1919. doi:10.1098/rspb.1998.0520

NOTE (to content thieves): this piece was originally published on The Guardian.

.. .. .. .. .. .. .. .. .. .. ..

When she's not out birding, GrrlScientist can also be found here: Maniraptora. She's very active on twitter @GrrlScientist and sometimes lurks on social media: facebook, G+, LinkedIn, and Pinterest.