New Website

I've got a website for my research up and running. It is a typical academic website, with links to research articles, contact info, etc. This blog will continue to highlight my work in progress, especially as it relates to Panama's birds. That website is: www.mj-miller.net

Delays in Posting

Too much time has passed since posting. We had a relaxing trip to the states earlier this month. The highlight was seeing U2 in concert in Boston! Frustratingly, upon our return to Panama, some one decided to break into our house and steal both laptops. It's taking me a while to get back to speed.

Nonetheless, our work with avian disease is growing rapidly, and I'm trying to juggle that with the on-going work in the diversification and speciation in Panamanian lowland birds. It should be a fun year ahead.

Just Back from the 127th Annual Meeting of the AOU

I just returned from Philadelphia, where U Penn was hosting the 127th edition of the annual meeting of the American Ornithologists' Union. The meeting was shorter by a day that typical meetings -- the economy even affects already frugal ornithologists. But we had a productive meeting. It was good to be a representative of STRI, Panama, and Neotropical birds at the conference. Lot's of folks are interested in what we've been uncovering about Panama's cryptic bird diversity, and there was a few really interesting talks that shook things up a bit. For example we learned that Green Violet-ears from Panama northward are only very distant relatives of conspecifics in the Andes.

Joel Cracraft reviewed recent geological literature which, along with trumpeters (Genus Psophia) suggests that western Amazonian forests are the most recent of the Amazonian biome. I'm sure the tropical tree ecologists at STRI would have something to say about that, since western Amazonia is the most species rich place in the world not just for birds, but also for trees, beetles, dragonflies, primates, etc. And we generally believe that older biomes have more species than younger ones. It's no understatement to say that I think that this was among the most controversial of talks at the meeting. (Top honors goes to an undergrad from Cornell who presented compelling evidence for a much better tree of the relationship among North American chickadees...the old tree didn't make sense, but that didn't stop it's authors from raising issue with the 22 year old who presented the new phylogenetic hypothesis.

Finally, a note about Panama's birds. George Angehr as

ked me to look at specimens of the Emerald Toucanet from throughout Panama. According t

o genetic data, the birds from Darien are sister to all the other birds from Central America, including

those that have throat colors other than blue. Genetic distances are large, and the authors of that study want to call each form a separate species. They didn't have material from the central part of Panama, but assumed it lumped in with the western Panama form (caeruleogularis) and not the eastern from (cognatus). But, George thinks that the birds from El Valle, Cerro Campana or elsewhere in central Panama may have Darien characteristics. Dear Birder, you can help out! Field notes of Emerald Toucanets are helpful. We're looking for presence of a red dot on the base of the mandible and some day-glo sky blue around the eye. In Philadelphia, I compared 100 year old specimens from Boquete and northern Colombia and found that both marks werk pretty consistent among individuals. Hat tip to Nick Sly for the figure. Nick is another recent undergrad from Cornell that I hope will be visiting us for a short-term research project in Panama soon.

Do Hummingbirds Speciate faster?

I think that the evidence from the two studies below (here and here) suggests that they just might. (I'll show a third, and perhaps strongest case, from Selasphorus in a future post).

Next posts are going to look at some non-hummingbirds that I'm working on.

Re-assessing species limits for the Escudo Hummingbird (Amazilia handleyi)

Two weeks ago, I was fortunate to be invited to give a seminar to the Panama Audubon Society. I chose to talk about how molecular systematics can help inform questions of species limits. One of the examples that I used was the case of the Escudo Hummingbird, Amazila handleyi. The Escudo Hummingbird looks a lot like the Rufous-tailed Hummingbird (an Amazilia common in the lowlands of Central America that ranges from southeast Mexico to northwest Ecuador) but on steroids. Above is a photo of specimens taken by Michael Lelevier who is leading our collaboration on the phylogeography of Rufous-tailed Hummingbirds (D are Escudo Hummingbirds). The Escudo Hummingbird is endemic to Isla Escudo, a small island off the coast of Caribbean Veraguas, near the Bocas del Toro archipelago. There's a map below. The Escudo Hummingbird is quite clearly related to Rufous-tailed Hummingbirds, and the first scientific specimens of this taxon date to 1962. Notice that I'm calling it a taxon not a species, because that is the debate. Although Alexander Wetmore described the Escudo Hummingbird as a distinct species in 1963, noting both the size and coloration differences, subsequently this taxon has been down-graded to a sub-species of the Rufous-tailed hummingbird. Today, the American Ornithologists' Union (the official checklist for North and Central America) follows that classification (i.e. Amazilia tzacatl handleyi); the Panama Audubon Society maintains their own checklist, and considers the Escudo Hummingbird a full species (Amazilia handleyi).

As I pointed out to the Audubon folks, the Escudo Hummingbird

is the most physically distinctive member of the Rufous-tailed group, but not the most genetically distinctive (at least using mitochondrial DNA [mtDNA]). Within the entire complex, genetic distances are modest (less than 2%, or about a million years). Deep splits include the split between Central America and South America. There is also a relatively distinctive mitochondrial clade found most common on Isla Coiba but also fr

om one individual in Pacific Costa Rica. In contrast the Escudo Hummingbird is a little nub on a mass of closely related individuals from the Caribbean lowlands of southeastern Mexico all the way down to central Panama.

Isla Escudo is believed to have been connected to the Veraguas mainland during the Pleistocene, when sea levels were lower. The estimates that I have found in the scientific literature date its isolation to the Holocene (8900 years ago, to be precise...we'll get to these estimates later). So, my thinking up to the seminar was that the mtDNA data agreed with the isolation of a small founder population about 10,000 years ago. Do what you want with that, but unlikely to be a reproductively isolated population, which is my criterion for defining a species (there others, but I won't bore you with that debate).

But after the seminar I got to thinking about it a little more and I was bothered by something. You see, the I presented a figure of mitochondrial haplotypes (particular genetic sequences from a fragment of mtDNA) from the Bocas mainland, Isla Colon (in the Bocas archipelago) and Escudo. To the right is that image. Isla Colon and the Bocas mainland share

haplotypes, which is what we would expect given our understanding of the isolation of the Bocas archipelago: namely that they were also isolated during the

Holocene (albeit a bit earlier, i.e. as early as six thousand years and as recently as one thousand). Two populations share haplotypes for two reasons. The most obvious is gene flow. But two populations can not be currently genetically in contact, but still share haplotypes because their time in isolation is quite recent. For

example, if we sent one million people to Mars to establish a Martian colony, they would share our genes for considerable time, even if no rocketships went back and forth between

Mars and Earth. Only the slow accumulation of independent mutations would cause DNA sequences to be different.

We generally believe that avian mtDNA mutates at about 1% per million years. Therefore, two sequences that differ by 2% likely had a comm

on ancestor about 1 million year ago because each lineage was independently mutating at 1% per 1,000,000 years. So, the difference between 5200 years (the estimate for the age of isolation of Isla Colon) and Isla Escudo (8900 years) is essentially meaningless for mtDNA differences. So, given similar immigration patterns from the mainland, Isla Colon and Isla Escudo should have similar genetic profiles relative to the mainland, but they don't.

Isla Escudo is much further from the mainland than Isla Colon (17.6 km vs. 1.5), and is much smaller (4.3 vs. 59.0 sq. km.), so I simply chalked up the dif

ferences to les

s frequent immigration from the mainland and smaller population size (new mutations become fixed in smaller populations more quickly than in larger ones). But, population geneticists have gotten new tools to explore these issues in a much more robust manner. The ability to sequence massive amounts of DNA is one breakthrough that is revolutionizing systematic ornithology. Equally important is the use of Markov Chain Monte Carlo simulation techniques in super-fast computers that allow us to routinely do complex calculations of the probability of certain population genetics parameters that we couldn't even have imagined 15 years ago.

So, I used IM which is a software developed to do just that to estimate gene flow between Escudo and Isla Colon and the Bocas mainland. Not surprisingly, the result was no gene flow. IM allows the researcher to jointly estimate migration rates (i.e. gene flow) and divergence times between two closely-related populations. However, with limited data, precision on both the estimate of divergence time and gene flow are limited. But, because these analyses are Bayesian in nature, peeking at your data to refine analyses is OK. So I tur

ned off gene flow on a second run of the IM, and got some results that I should have realized before hand: the split between Escudo Hummingbirds and other Rufous-tailed Hummingbirds is much older than the Holocene isolation of Isla Escudo.

In fact, the split seems to be about 140,000 years ago. The

95% confidence interval on the estimate is 40,000 – 355,000 years ago; i.e. there is no way that the mtDNA differences date to the Holocene isolation of Es

cudo, they are an order of magnitude older (or our estimate of mtDNA mutation in Amazilia is an order of magnitude too low [quite unlikely]. To the right I show the graph of estimated divergence time (x-axis) vs. probability (y-axis). Note the mass of probability around 150,000 years ago.

And, the IM model assumes migration since divergence begins. So, Escudo Hummingbirds had at least 30,000 years (and probably more like 130,000 years) to exchange genes with other Rufous-tails before become isolated on tiny Escudo Island. Shockingly, I think that the evidence accumulated points not to the Holocene isolation of typical Caribbean Rufous-tailed Hummingbirds, but the preservation of a much older lineages as a relictual population found no where else.

During the late Pleistocene sea-levels waxed and waned. At lows, such as those from the Last Glacial Maximum (around 18,000 years ago) until the start of the Holocene (around 10,000 years ago) what ever was the range of the ancestor of modern Escudo Hummingbirds should have come contact with Rufous-tailed Hummingbirds and if they were the same species, should have exchanged copies of mtDNA. The small size of Escudo means that evidence of that contact might likely have vanished during the last 10,000 years. However, if that occurred, we should have observed Escudo haplotypes in mainland individuals (even in only 1 or 2 individuals). We did not. In fact we have sequenced over 90 birds from mainland Central America, and none have the Escudo haplotype.

It's time to revisit the biogeography of Escudo. In 2003, our lab at STRI published a paper in the Condor (Gonzalez et al. 2003) on Bay Wrens. They observed two unique, but distant haplotypes on Escudo Island (the Bay Wren on Escudo is quite distinctive from the Central American Bay Wrens). Both Coiba and the Pearl Islands are living museums of prehistoric avian diversity in Panama (the Coiba Spinetail exists no where else on Earth, and the nearest conspecific of the White-fringed Antwren on the Pearl Islands occurs in northern South America). In the meantime, it's time to give the Escudo Hummingbirds the distinction that it deserves, as a full species.

Anthracothorax Mangos in Western Panama

What's going on with Mango hummingbirds in western Panama?

Current taxonomy recognizes three species of Mango hummingbird in Central America. Most experts agree with the following schematic for the distribution of these species.

The Green-breasted Mango (Anthracothorax prevostii) is found from southern Mexico to northern Costa Rica, and also Bocas del Toro Panama. Black-throated Mango (A. nigricollis) is found throughout much of the tropical lowlands in South America but can also be found in eastern Panama westward until the Canal Zone. A third species Veraguan Mango (A. veraguensis) has been described from the Pacific lowlands of western Panama and adjacent Costa Rica.

It is important to note that this is a short-hand simplification of a known taxonomic problem. What is actually going on is much more complicated, and largely unknown. Such problems are quite common in most taxonomic groups, but much less so in birds, because of the historical efforts of bird specimen collectors to document bird variation throughout their range. Ornithologists have solved the vast majority of these problems. But lack of specimens and/or research effort has left a few. Sometimes, new tools such as DNA sequencing and/or comparisons of bird vocalizations have provided  important clues. A good, recent example from North America are the two Empidonax species that until the 1989 AOU checklist were considered "Western Flycatcher".

In the case of the Mangos, University of New Mexico PhD student Michael Lelevier and I are looking at the plumage and DNA of the Mangos from western Panama at the same time to try to understand species limits in this area. We have found a correlation with Veraguan vs. Green-breasted type plumages and very shallow, subtle DNA variation in the VERY, VERY limited number of samples that we have available.

In the above picture, we compare a known male Green-breasted Mango (from Mexico) to three males from Chiriqui. We can see that two of the three Chiriqui birds have a deep indigo patch on the throat that extends to the upper breast. Such a patch is shared with the Green-breasted Mango. In contrast, the third individual does not show such a blue/black patch (note that the darkness in the extreme upper throat is an effect of shadowing, and under better light is glittering green; the colors in these hummingbirds are from structural pigments so the angle of the observation affects the color observed). This third individual has plumage characteristic of Veraguan Mangos. It should be noted that all three of these Chiriqui birds were collected on the same day at the exact same site over a period of two hours in a windbreak near Remedios; thus any differences are not due to geography.

When we classify all existing specimens of Mangos from western Panama that have a museum skin voucher specimen and an associated tissue allowing DNA-based studies (a total of 17 individual birds collected during the last 30 years), we find the smallest possible variation between the two plumage groups (All Chiriqui birds were collected by Michael and me, and classified to plumage by Michael; birds from Bocas were collected in the late 1980

s by Smithsonian scientists from

 Washington DC, who provided the plumage-based classification. In fact the variation (two mutations, see the big red arrow) is the same as what we find within individuals of the same plumage type. In fact, there is one Chiriqui bird with Green-breasted plumage that varies by 5 mutations from other Green-breasted Mangos. Also note that the two shared mutations that help to discriminate Green-breasted from Veraguan plumages are found in geographically remote populations in Mexico and Belize.

What does this mean? If the two are separate species, they are incredibly young. Most sister species of birds are between 2% - 10% different from one another using the DNA marker that Michael and I are using here. That would mean 20 - 100 mutations (since our DNA fragment is about 1000 bases long). Therefore, if we have two different species, we are talking an order of magnitude less difference than what is "normal". Also, it means that there is no genetic barrier to inter-breeding between the two forms. Up to about 15% differences, different bird species can readily hybridize, and much below 4%, they are so compatible that it is possible for one species' genes to swamp another. This is currently going on in Blue-winged and Golden Winged (Vermivora) Warblers in North America. Any reproductive isolation would have to involve mating displays or other behavior since the two plumage types ARE NOT geographically seperated (contra the earlier schematic). 

Alternatively, speciation was interrupted. Speciation might take a million years or more; the genetics tells us that the split between Veraguan and Green-breasted Mangos is 100,000 years or likely much less (since we expect 2% variation per million years, however you should subtract the level of within population variation to correct for natural variation that occurred...doing so would leave you with an estimate of 0 years since splitting. The true date is somewhere much less than 100,000 years ago). If this is right, than it isn't fair to characterize the Mangos of western Panama as either Veraguan or Green-breasted, they actually would be a little of both. (I know that this is troubling for twitching life lists...and future posts are going to address this with Jacanas and many other birds from Panama. I hope that ultimately this information makes time spent watching Panama's birds more fulfilling, even if it costs a few twitches).

How do we seperate between the two possibilities? First, it would be great to have more specimens. The taxonomy of these guys is based on the 17 birds that we sequenced and only a dozen or two more that were collected before the days of DNA science. We will need to punt until we get more material. If we do have more material, we can use other DNA tools to more finely characterize gene flow between the forms. At the same time, field observations of mating behavior are perhaps equally critical. Ideally we'd geneically characterize birds attempting to mate to measure the extent of mate choice, but if you've spent any time watching these birds, you know how operationally difficult that will be. Additional genetic data should point us in a better direction.

I hope to provide a similar snippet of my on-going research using this blog on a weekly basis. Up coming notes are being worked up for Selasphorus hummingbirds of western Panama, Snowy-bellied Hummingbirds, Mionectes flycatchers and Schiffornis, as well as I hope some quite novel data on Red-capped and Golded-headed Manakins from eastern Panama.