Notes from on-going research on Neotropical birds

Photos of a Glow-throated Hummingbird Specimen

2011-01-05T10:19:00.000-08:00

George Angehr sent me photos of a a specimen of Glow-throated Hummingbird (Selasphorus ardens) from the American Museum of Natural History. The Glow-throated Hummingbird is on the right; on the left is a Scintillant Hummingbird (Selasphorus scintilla). This updates my earlier post of the plumages of the southern species of Selasphorus. I can see how folks might confuse a Glow-throated Hummingbird with a Volcano Hummingbird. Check out the earlier post for all the details.

More Jacana Hybrids

2011-01-01T07:11:00.001-08:00

Here are some more jacanas from western Panama. These birds are not yet prepared as specimens, and before we do that, we'll be careful to document with photos the facial ornamentation. I've got the photo in better quality on my website. However, what you can see is that the right most pair of birds appear to be Wattled Jacanas, to the left appears to be a pure Northern Jacana, and then the three leftmost birds are clearly hybrids, as they have facial ornamentation scrambled between the two species.

The apparent fact that both pure species are intermixing in the hybrid zone, rather than a hybrid zone where most birds are hybirds (as occurs in many other avian hybird zone) suggests that there is a fitness consequence to hybridization. Again, my hunch is strongly that it is cultural rather than intrinsic (see my earlier post). But at least we have confirmation of the hybridization, and a field site to begin monitoring behavior. Next step is to genotype these fresh birds. A great way to start the New Year. Again, check my earlier post, and again I will be collecting your observations of Jacana populations from western Panama to make a detailed map!

Updates

2010-12-23T16:59:00.000-08:00

It's been a long time between posts. Lots of stuff was going on over the past few months personally, so I was quiet, but now that is behind me, and so it's time to get to the news.

First, we've got the mosquitoes sorted and identified to species from our CDC work in the canal watershed and in eastern Panama where we had the encephalitis outbreak. It was back-breaking work for Jose Loiaza who had to identify tens of thousands of mosquitoes. After the holiday break, I will apply for an export permit for these mosquitoes so that the CDC can survey them for diseases.

Secondly, we are training two new Panamanian students in field ornithology and specimen preparation. I'm quite happy about this development, because it means that we are going to have a productive dry season.

Finally, our collaborative group has been funded for another disease project, this time with ticks. It is another opportunity to understand

the relationship between deforestation and disease transmission, since ticks carry Rickettsia, a group of bacteria that are responsible for many diseases such as Rocky Mountain Spotted Fever, Africa tick bite fever, etc. Rocky Mountain Spotted Fever, despite its name, has b een known from Panama since the 50's, and recently killed a four year old girl in the canal watershed in 2004. Our current grant provides seed money to develop the Smithsonian's capability of leading research on the intersection of biodiversity and emerging disease, approaching the question from a more holistic, theoretical, and biologically-driven approach than typically undertaken by disease scientists.

I want to point out that our bird group is positioned well to lead these questions because of our commitment to saving everything possible from our specimens. Our earlier CDC project funded us to look at blood-bourne viruses, but because we want to archive all biological material from bird specimens, we've preserved ecto-parasites from our birds. This is the point of biological collections: to archive material for questions that remain to be asked. One only wonders what other knowledge is to be gained from our specimens!

A tale of two Jacanas

2010-12-21T12:43:00.000-08:00

This story comes to me by way of Neal Smith, emeritus Staff Scientist at the Smithsonian Tropical Research Institute, an observant naturalist, a rabid consumer of scientific literature, and a first rate gentleman.

One day I was in Neal's office, which is a treasure trove of Panama artifacts, tattered maps, dusty photos, and to my surprise, many biological specimens. I came that day to see jacanas. Neal was quite excited to show me some jacana specimens from western Panama.

It is a curious thing, because "odd" jacanas have been popping up in the conversations of Panamanian bird enthusiasts. These often get posted with photos at the Xenornis blog. Here is a photo of a bird with brown dorsal plumage and a weird facial helmet. Here is another example of a "wattled" jacana with a brown dorsal plumage from Gamboa. The birdwatching community is fairly confident that these are vagrant Wattled Jacanas from South America (in much of South America, Wattled Jacanas have brown dorsal plumage).

However, I think I can demonstrate that these birds are in fact hybrids between the Northern and Wattled Jacanas, rather than odd plumages or vagrants from South America. First a review of the two species of jacana in the Americas.

1. Northern Jacana. Found along both coasts of Middle America from near the Texas border south to extreme western Panama on both coasts, as well as in the West Indies. In Panama, it is clearly abundant in Bocas del Toro, its distribution in the Pacific lowlands of Costa Rica and Panama is less clear, probably because there is much less standing water. The Northern Jacana has black and brown plumage with a yellow tri-lobate facial shield and a blue skin patch over the base of the bill.

2. Wattled Jacana. From central Panama south throughout South America. The key identifier of a Wattled Jacana in the Americas is the red bi-lobate facial shield with droops that extend like a handlebar mustache. Birds from Panama have all black plumage, but populations in certain parts of South America have the black and brown plumage pattern found in Northern Jacanas. In fact, most of the South American populations, and in fact all east of the Andes have that plumage. But the Andes are a bit hard for birds to cross (shameless promotion of one of my papers).

So what are these "odd birds". Well, first we need to think about the geography: these sightings are right around where we might expect the two species, Northern and Wattled, to meet. Second, if we look at the literature, we see that hybrids have been discovered for nearly 40 years (Betts 1973: The Auk). (I'm really not sure what the Jenni and Mace [1999] were talking about in Birds of North America online: "No definite hybrids are known, contrary to frequent citation

s of hybridization. Several specimens with intermediate shields or plumage were described aspossible hybrids from Veraguas, Panama (perhaps same specimens; Hellmayr and Conover 1948, Wetmore 1965), and from Osa Peninsula, Costa Rica (Betts 1973). These are possibly just young birds." Not true at all: Betts shows a nice photo of an adult female with red, yellow and blue facial shield and RICTAL WATTLES (that's what I'm calling the handlebar mustache).

Well, what Neal had in his office I think really seals the deal. Apparently Steve Emlen, from Cornell, collected a series of Jacanas from western Panama in the mid-1990s. These jacanas clearly show mixed assemblages of the facial ornamentation of the two species (along with the plumage typical of the Northern Jacana, but drabber, and with much less distinction between the brown and black regions that one would find in a proper Northern Jacana).

I couldn't get big fotos on this blog, so I'll redirect you to my website for the photos. In the first two photos, you can see a Northern Jacana compared to a Wattled Jacana. Note the three lobes in the Northern versus the two lobes and the long rictal wattles (handlebars). In the second set of photos you can see hybrid jacanas compared to a proper Wattled Jacana. Note that the rictal wattles are reduced, and the specimen label notes that the shield had tinges of blue throughout a very palid red (rather than the bright red of a Wattled Jacana). Also, note that the shields are reduced and some are tri-lobate (like Northern Jacanas) rather than the bi-lobate form of Wattled Jacana. In the final picture, you can see the variable nature of the brown plumage on the underparts, and you might find that it's easier to see the reduction of the rictal wattles.

Hybridization in the eight species of jacanas (the remaining six species are found in the Old World) is unknown except for Wattled and Northern. Likewise, Wattled and Northern Jacanas have often been classified as conspecific. Below is a a small phylogeographic tree of the two species. The data come from the DNA barcode (COI) region, a small section of mitochondrial DNA.

The first thing that you should note is that there is consistent genetic differentiation between Wattled (J. jacana) and Northerns (J. spinosa). This is what you would expect to see if the two forms were really separate species, though this doesn't PROVE that they are distinct species. (But with the hybridization data, it makes a strong case, more on that below). Secondly, the is little genetic variation in either species across their sampled ranges, and none of the variation is geographically structured. That suggests that each species is able to maintain gene flow over long distances, and that maybe the species are relatively young. The final thing that you should notice is that the degree of genetic differentiation between the two species is small (about 1.5%), which confirms that they split recently, and falls within the range that we expect hybridization to be possible (several studies have show that there are genetic incompatibilities that make even successful hybrids inviable after about 7-8% differentiation).

The fact that Wattled Jacanas from Cocle have Wattled Jacana mtDNA and Northern Jacanas from Chiriqui have Northern mtDNA suggests that the species boundary is relatively robust between these two forms. Ornithologists used to think that if there was hybridization, then "speciation was not complete", and therefore called the two forms subspecies. We now know that a narrow hybrid zone where genes come in but don't leak beyond the narrow hybrid zone is a fairly common stage at the tail end of the speciation process, and that for most of the individuals in each species, species-specific genetic cohesion is maintained. So I think that it's fair to say that the hybridization actually substantially bolsters the argument that we've got two reproductively-isolated species here.

But that final part is where things get interesting, and where I hope to have a student working on this question next year. First, we need to improve our sample of mtDNA to demonstrate that outside the contact zone that species-specific genetic cohesion is maintained (sample of one and three don't exactly pass muster in peer review). Secondly, what is the genetic composition of the hybrids? Do they always Northern mtDNA, which would suggest a mating of a Northern female with a Wattled male, since mtDNA is transmitted only by mothers, or do they only have Wattled mtDNA, which would suggest the reverse? Often we find unidirectional hybridization, that is either because one species is demographically much larger than the other, or because one species prefers mates of the other. Such is the case in the Manacus hybrid zone in Bocas del Toro, where candei females prefer the golden plumage of vitellinus males over the white collars of the males of their own species.

One of the interesting aspects of jacana biology is that they have a curious polyandrous mating system. Females have harems of males. Each male receives a clutch, but it may or may not be its offspring that he cares for (This comes from Steve Emlen's paper in Proceeding of the Royal Society published in the late 90s; their study population was in Gamboa: there is a nice PBS movie about this research). From the female perspective there is little disadvantage to hetero-specific mating (i.e. across species lines), compared to most bird species where the female gets only one clutch per season and so therefore much be much choosier about her mate. This may facilitate the hybridization. So my student will need to do some behavioral ecology to get at this question too.

Finally, what limits the gene exchange among jacana species? There must be something going on because Jacanas don't make a hybrid swarm where the two species are completely blurred and we can't draw limits to species.

Because mitochondrial genes are passed through the female line, and in birds, unlike mammals, females are heterogametic (i.e. have the two different classes of sex chromosomes) mitochondrial DNA might have a much harder time crossing the species boundary compared to nuclear DNA. This is because of the phenomenon of Haldane's Rule, which observes in hybridization the heterogamic sex suffers the consequences of hybridization more severely than the other sex....thus we observe only female mules, because any male offspring of a horse X donkey mating are inviable and are aborted. If Haldane's Rule is operative, and there is no reason to think that it isn't, we should observe that most hybrids are male (which we would need to do during the preparation of museum specimens, since sex organs are inside birds), and perhaps more interestingly, we should also observe that nuclear DNA is moving quite handsomely between the two species since hybrid males may successfully be mating and backcrossing, bringing a half a genome's worth of heterospecific DNA into the backcross.

However, there are two ways that the breeding system might actually put the stops to the introgression of heterospecific genes. First, imagine that a male rears his clutch, if it is clearly conspecific, he doesn't know whether or not the clutch is his. But if it is a hybrid clutch he can be pretty sure that it isn't his, and perhaps his care is reduced, or the clutch is abandoned, or perhaps even killed. Again, this is where observations are important. Secondly, we've seen that the secondary sexual traits of hybrids are under-developed (the facial shields and wattles). Perhaps hybrid males are "unlucky in love" as it were, and since it is likely hybrid males that are the engines of backcrossing gene flow (backcrossing being the means of getting heterospecific DNA into the parental population), then if they don't mate often, they are "socially sterilized" rather than intrinsically sterile.

There's a lot of interesting biology yet to be discovered in the jacana hybrid system, but the first thing that we need to do is map the hybrid zone. So, when you are out birdwatching, I beg you to pay some attention to the flocks of Jacanas that you see. Both kind of data points are considerably useful: if you only see Wattled or Northern that is as useful as if you see mixed flocks. If you can email me (millerma AT si DOT edu) with your sighting, I'll update this posting with a map of your points. This is a great opportunity to do some citizen science here in Panama!

The guide to plumages in the southern Selasphorus

2010-09-29T12:07:00.000-07:00

I had an opportunity to visit the US National Museum in Washington DC earlier this month. As I've said before, I have an interest in the historical biogeography of the the species of Selasphorus that are found in Costa Rica and Panama. There's a lot ofconfusion about species limits and plumage patterns. Here's a quick guide.

The current, definitive taxonomy of this group comes from Gary Stiles's 1983 article published in the Auk. That article can be freely accessed on line from the SORA collection, here. Stiles notes the following taxa:

Selasphorus flammula (Volcano Hummingbird) with three subspecies

flammula (endemic to the Irazú and Turrialba volcanoes in Costa Rica)

simoni (endemic to Volcán Poás in Costa Rica)

torridus (the most widespread form, througout the Talamanca range in Costa Rica and Panama)

Selasphorus scintilla (Scintillant Hummingbird) with one subspecies

Selasphorus ardens (Glow-throated Hummingbird)

with three subspecies

It's important to note that prior to Stiles's work, no one was certain of the relationship amongst the three subspecies of Volcano Hummingbird,

and often it was considered that one or two of these subspecies as actually related to either the Glow-throated or the Scintillant (for reasons that will make sense when you look at the photo to the right). Gary focused on morphological characteristics to determine species limits. And from looking at dozens of prepared study skins, Gary found that throat color not withstanding, he could lump the specimens into three bins (flammula, scintilla, and ardens).

So, above, I present a figure of the three plumages of the Volcano Hummingbird, and the Scintillant Hummingbird. I don't show the Glow-throated Hummingbird, because the US National Museum didn't have any specimens (at least male specimens). There aren't vary many specimens of Selasphorus ardens (Glow-throated) out there; so perhaps George Angehr can get a photo the net time that he's at the American Museum on Central Park West. Based on field guides and George's description of the Glow-throated Hummingbird, it must look a lot like the simoni race of Volcano Hummingbird.

And there is an apocryphal account of a Selasphorus from the top of Cerro Hoyo, with no surviving specimens, that might very well be another species lost to science. Obviously, I don't have a photograph of that one either.

Some Updates

2010-09-16T06:47:00.000-07:00

Wow, it's been a very hectic few months. The guys did great in eastern Panama, and with our collaborators both at the Gorgas and in abroad, I think that we'll have some new and important information about the ecology of these encephalitis outbreaks. We collected about 8,000 mosquitoes, many with blood still in their abdomen. And we collected blood samples from a wide diversity of bird species. Equine Encephalitis is usually quite lethal to horses, but because of its lethality, horses are considered dead-ends in the transmission cycle; they simply die too quickly to be bitten again and pass on the virus via a vector to another host. Instead, there is another organism that must serve as the "reservoir" for the virus. Perhaps it's most likely that the reservoir is small mammals (e.g. rodents), but it's possible that the reservoir is some bird species.

We will tackle this principally by looking at which mosquitoes have virus isolates inside them, and then trying to figure out who those mosquitoes bite. By sequencing the DNA inside mosquito blood meals (vertebrate blood meals inside the mosquito abdomen) from infected vector mosquito species, we should have a better idea of who serves as the reservoir. At the same time, our bird blood samples should test positive for encephalitis antibodies if birds are an important part of the encephalitis transmission cycle.

Team Working on Encephalitis Outbreak

2010-06-15T14:23:00.001-07:00

It is with great pride that I bid farewell to Oscar, Alonso and Celestino this morning. They left with Jeremy Ledermann of the CDC and scientists from the Animal Health lab of the Agriculture Ministry (MIDA) to help collect samples in eastern Panama.

Here in Panama, the rumors have gotten ahead of the scientific facts, but I got the straight skinny from the Alex Martinez, my colleague and head of virology at the Gorgas. Basically, there appears to be an outbreak of either Venezuelan or Eastern Equine Encephalitis. One girl, nearly the same age as my daughter, has already died, and many horses have died.

The team is currently near Tortí and will move from there to the Metetí area. We'll be providing the Gorgas will all of the diagnostic samples. There are claims of dead birds in the area, but I should caution that there's lots of mis-information out there in a population that has been historically marginalized and is quite reasonably quite afraid.

STRI's role in this research is multi-faceted. Jose Loaiza will return from defending his PhD in medical entomology from McGill University and will identify the mosquitos collected. They will be then screened for virus, which we hope to sequence in order to tell us where the virus comes from. Blood serum samples from birds in the affected area will be screen for VEE and EEE antibodies. Together we will put this information together to try to understand the ecology of this outbreak. This is quite important because "migratory birds" were immediately blamed for the disease.

Typically, when an outbreak occurs, the conventional wisdom is that the virus was carried into the region somehow. Birds, especially migratory birds, are a convenient scapegoat. However, it may be that the virus has historically persisted as in a local reservoir. Hopefully with the combined study of the small rodent populations (sampling being done by MIDA) and the bird and mosquito populations (our group), we will be able to identify which animal species are part of the transmission cycle.

This is one of the strongest arguments for why we return to the same region year after year to collect specimens. Tissues from museum specimens provide a very useful source of information about the baseline conditions. Had we sampled previously in Metetí and Tortí, we would be able to evaluate changes in the serological condition of birds collected before the outbreak to those collected during and after the outbreak. Thanks to our CDC funded work in the Panama Canal watershed, we will have this baseline information for the center part of our country.

Updates on the Escudo Hummingbird Question

2010-01-14T06:53:00.000-08:00

The new year starts with an intern, Andrea Baquero, who hails from Colombia working in the lab with me. This week we began to collect nuclear DNA fragments from Amazilia hummingbirds (tzacatl on the mainland and Isla Colon) and handleyi (Isla Escudo) to get a more robust estimate of divergence time and gene flow between Escudo and the mainland. We haven't analyzed the preliminary data yet, but the few sequences that I've seen give me the general impression that gene flow was ceased between Escudo and the mainland for some time now.

I have to say that I'm pretty surprised at the level of DNA polymorphism in the Escudo population. Polymorphism is another word for genetic diversity, and as everyone remembers from high school biology, small inbred populations lose genetic diversity overtime due to genetic drift. However, we only have two small nuclear DNA fragments (as opposed to the mitochondrial DNA fragments I discussed earlier) and so this may be a consequence of chance. We will be collecting more data in the coming weeks, and I'll post an update.

I believe that this would make the Escudo Hummingbird, among all the world's hummingbirds, the species with the smallest range.

New Website

2009-10-03T09:09:00.000-07:00

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

2009-09-29T23:28:00.000-07:00

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

2009-08-18T17:21:00.000-07:00

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?

2009-06-22T13:21:00.000-07:00

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)

2009-06-22T07:38:00.000-07:00

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

2009-04-22T11:49:00.000-07:00

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.