AUTHOR BLOG: How do traits change across a scrub-jay hybrid zone?

Devon DeRaad

Linked paper: Phenotypic clines across an unstudied hybrid zone in Woodhouse’s Scrub-Jay (Aphelocoma woodhouseii) by D.A DeRaad, J.M Maley, W.L.E. Tsai, and J.E. McCormack, The Auk: Ornithological Advances.

Devon DeRaad lines up Woodhouse’s Scrub-Jays (left) and Sumichrast’s Scrub-Jays (right) to compare back color between the forms. Photo by John McCormack.

Where should we draw the line between species? Biologists have debated this question for over 100 years. For much of that time, Ernst Mayr’s Biological Species Concept, which defines a species as a group of individuals that is reproductively isolated from other groups, has dominated the conversation. The BSC, as it has come to be abbreviated, led to more conservative species definitions, with many distinctive forms lumped together as single species because of actual or even potential interbreeding. Recently, however, more and more evidence of hybridization between species has accumulated, especially in birds. The question now is often not whether there is gene flow between what we would consider species, but how much is too much for them to still be considered separate? And when gene flow happens, how does it affect the array of traits that we can see in hybridizing forms?

The New World Jay genus Aphelocoma – which includes well-known species such as the California Scrub-Jay (A. californica) and the Mexican Jay (A. wollweberi) – has proven to be a good study system for investigating the role of gene flow in the early stages of speciation. Because Aphelocoma species don’t tend to move around much, many geographically-isolated, locally-adapted forms have evolved, but they have not become so different that they don’t hybridize when they come into contact with each other. Several of these contact zones have been well studied, like the one between the California Scrub-Jay and Woodhouse’s Scrub Jay (A. woodhouseii), which used to be considered a single species called the Western Scrub-Jay. In fact, the species was split based in part on the fact that although gene flow was occurring, it seemed to produce traits that were selected against outside of the small area where the two groups overlap and hybridize.

I was an undergraduate researcher at the Moore Laboratory of Zoology at Occidental College when I learned of another, largely unstudied Aphelocoma hybrid zone, between the northern form of Woodhouse’s Scrub-Jay and a distinct southern lineage called Sumichrast’s Scrub-Jay. The largest collection of Mexican birds in the world, the Moore Lab has an extensive collection of Woodhouse’s Scrub-Jay specimens from throughout Mexico. Using this valuable collection as well as specimens loaned from other natural history museums, we set out to discover whether there really was evidence for gene flow between these two groups and, if so, how much.

I measured the tail, wing, tarsus, bill length, bill width, and bill depth of 133 specimens from throughout Mexico. I also measured the intensity of blue on the back feathers of each specimen with a spectrophotometer, a tool that captures the wavelength of light reflected off of a surface, as back color seemed to be a major difference between the two forms. Our results confirmed that Sumichrast’s Scrub-Jay is significantly larger and has brown back feathers, as opposed to the blue-gray back feathers of Woodhouse’s Scrub-Jays from northern Mexico. A new analytical method for visualizing geographic transitions in traits called HZAR also showed that while body size transitioned gradually, the transition in back color was much more rapid, suggesting potential selection on this trait.

We were excited by our results not only because it was fascinating to see two traits, size and color, behaving differently across a hybrid zone, but also because the confirmation of the hybrid zone presents another opportunity to study speciation in action in Aphelocoma jays. And while we’re proud to publish a study on hybrid zones that does not include genetic data, providing another example of the modern value of museum specimens in their own right, we do hope to collect more specimens from the contact zone in the future and use genetic data to see how the genomes of both forms are responding to hybridization. These future genetic studies, combined with behavioral, vocalization, and ecological data, will provide an integrated portrait of these divergent lineages that have come back into contact and will help us make an informed decision about how best to recognize the taxonomic distinctiveness of these lineages—that is, whether the species once known as the Western Scrub-Jay should be split yet again.

AUTHOR BLOG: Tracking cultural evolution in House Finch song, Part 2

David Lahti

Linked paper: Four decades of cultural evolution in House Finch songs by C. Ju, F.C. Geller, P.C. Mundinger, and D.C. Lahti, The Auk: Ornithological Advances 136:1, January 2019.

(Read part one here.)

So what did we learn about how House Finch songs have changed since the 1970s—the equivalent of a millennium of cultural evolution in human terms? Here are the main results, and how we interpret them. We have to be careful with interpretation, though, as we cannot be sure that the differences we observed represent consistent trends; it’s possible that the birds have been fluctuating through the years and we merely caught two random points.

  1. All the main features of House Finch song in 2012 (such as song length, pitch, and syntax) are within the same range as they were in 1975.

Because the basic characteristics of House Finch song have remained consistent across the decades, birds today would probably still recognize old recordings as being from their own species. We’re soon going to test this to find out for sure!

  1. Roughly half of the individual syllables that were around in 1975 were around in 2012, too. The more common the syllables were in 1975, the more likely they were to still be in use by 2012.
  2. However, none of the particular songs (that is, sequences of syllables) that we recorded in 1975 were sung by any bird in 2012.

These results are to be expected. Since House Finch syllables are learned whole, they can be preserved from generation to generation; perhaps birds even reinvent the same syllables over time. However, young birds individually assemble syllables into songs each generation, and there are millions of combinatorial possibilities.

  1. The population of songs is more diverse (there are more different syllables in use) in 2012 than there were in 1975.
  2. Although birds shared songs with each other in 1975, the birds in our 2012 sample didn’t share any songs with each other, despite being the same distances from their neighbors.

We know that the population of House Finches generally grew and expanded between 1975 and 2012, although a nasty outbreak of conjunctivitis was decimating the population for a while. A larger population means more neighbors to listen to and more individuals to create new syllable modifications as they learn. Both of these factors should eventually cause greater overall song variety, which is what both of these results show.

As is typical in science, we also found results we cannot readily explain:

  1. Birds in 2012 do not repeat their songs as reliably as they did in 1975—they are more likely to skip syllables, add new ones, or switch them around.
  2. Individual songs in 2012 have fewer different kinds of syllables than they did in 1975 (despite there being more total syllable types in use in the population as a whole!).
  3. In 2012, the syllables that are more common tend to be the ones that are more complex—they change pitch more rapidly and more often. They also tend to be higher pitched. This was not the case in 1975.

We’re developing some ideas to explain these curious results—hypotheses that will inspire our next round of field and laboratory work. The House Finch researchers in our lab are taking some exciting next steps, looking at such things as song similarity over geographic distance, changes on islands, early song development, social networks, and sex differences.

Unfortunately, Paul Mundinger passed away while this study was being conducted, and he never got to see the results. But it is because of his early work that we were able to chronicle changes in these songbirds over nearly four decades, and his song recordings (which are voluminous) will continue to provide us with interesting baseline data and prompt new research for years to come.

See more about the Lahti lab at http://lahtilab.org.

HawaiianHouseFinch
Photo by César Castillo.

AUTHOR BLOG: Tracking cultural evolution in House Finch song, Part 1

David Lahti

Linked paper: Four decades of cultural evolution in House Finch songs by C. Ju, F.C. Geller, P.C. Mundinger, and D.C. Lahti, The Auk: Ornithological Advances 136:1, January 2019.

The first bird song I ever recorded was that of a House Finch. When I was a kid growing up in Leominster, Massachusetts, the bird that nested behind my front porch lamp would fly out to a particular birch tree or the telephone wire and belt out a complex four-second warble over and over again. That sound became emblematic of summertime for me and my siblings. One day when I was in my room holding my tape recorder against the radio speaker to record songs (human songs, that is!), I heard the little red fellow outside start doing his thing, and I promptly stuck my recorder out the window for an acoustic memento. I actually ran across this cassette tape for the first time in nearly four decades a couple of months ago, coincidentally just as my first scientific paper on House Finch song was about to be accepted for publication in The Auk.

Here are a couple of examples of House Finch song. Read it like sheet music, with time on the horizontal axis and pitch on the vertical—it’s composed of a bunch of notes, or syllables.

House Finch Song 1
House Finch Song 2

The reason my research collaborators and I are interested in House Finch songs today is because these songs change over time and space—we’d like to know how and why they change the way they do. Most animals simply inherit the noises they make, and so the sounds don’t change much from generation to generation. About half of the world’s birds, however, learn how to “speak” as juveniles from older members of their own species, just as we humans do.

The youngsters don’t always imitate perfectly the songs they learn, and so over the generations small changes in these songs can accumulate. These changes result in noticeable song differences across time and space, just as we humans diverge in our accents and languages. For this reason, bird song is an important animal model system for the study of cumulative change in socially learned traits, what’s known as “cultural evolution.”

Long-term changes in bird song are rarely studied, because research projects don’t often last for decades. However, even as I was listening to that House Finch from my bedroom, Dr. Paul Mundinger, a professor at Queens College at the City University of New York, was recording them on western Long Island, in high quality and accompanied by meticulous field notes. Paul had just published a paper in The Condor showing that House Finches can have different song dialects. He had also indicated that young House Finches learn their songs by listening to a bunch of singing neighbors and assembling chunks of syllables from several of them, like an acoustic collage. The end result is two to four songs that an individual will sing consistently for the rest of its life.

Fast forward 37 years, and I, a new professor at the same college, became Paul’s friend and colleague. He was pleased to hear that I wished to pick up where he had left off with House Finch song in the 1970s (after which he had moved on to research on the canary). I was excited to compare his early House Finch recordings to the songs sung by local birds today. Because birds’ generations are so much shorter than those of humans, this would be like comparing our English to that used a millennium ago in the epic story Beowulf, which is so different from our modern language that it would be unintelligible to most English speakers today.

The main two steps in this study would be (1) to see what songs these Long Island House Finches are singing today, and (2) to find a reliable way to compare songs across time. Two doctoral students in my lab stepped up to the task. Franny Geller loves observing and recording birds, and so she recorded as many House Finches as she could find in western Long Island in 2012, and Chenghui Ju is a computational wiz who programmed software specifically to characterize and compare House Finch songs in different times and places. This study became part of Chenghui’s recent doctoral dissertation.

What did we learn? Find out in Part 2!

AUTHOR BLOG: How to hide a godwit—the story of Marbled Godwits in Alaska

Dan Ruthrauff

Linked paper: Flexible timing of annual movements across consistently used sites by Marbled Godwits breeding in Alaska by D.R. Ruthrauff, T.L. Tibbitts, and R.E. Gill, Jr, The Auk: Ornithological Advances 136:1, January 2019.

Dan Ruthrauff_MAGO 8Y UgashikAK
A newly banded Marbled Godwit. Photo by Dan Ruthrauff.

Marbled Godwits are common and conspicuous North American shorebirds. On its prairie breeding grounds, the godwit’s raucous call and proud flight display alerts all to its presence, and the species is equally obvious on its temperate nonbreeding grounds along both the Atlantic and Pacific coasts due to its gregarious nature and telltale alarm call. So how did such a charismatic species go largely undetected in Alaska until the 1980s?

The reason lies in this unique subspecies’ far-flung breeding range and cryptic occurrence across the state. Dan Gibson and Brina Kessel first described the Alaska-breeding subspecies Limosa fedoa beringiae in a 1989 research paper in The Condor. The authors pieced together information from anecdotal observations and a handful of specimens collected at a remote site on the Alaska Peninsula and combined this with evidence from museum specimens to define the subspecies, broadly describe its range, and ponder its migratory movements.

Fast forward thirty years, and we’ve learned surprisingly little about this subspecies, which is believed to number only about 2,000 individuals. Dan and Brina’s publication served as a touchstone for subsequent research on the subspecies, most of which has focused on the region surrounding Ugashik Bay on the Alaska Peninsula. Accessible only by plane or boat, this region has fewer than 200 human inhabitants across an area about half the size of Connecticut, a fact that helps explain why this brightly colored, boisterous shorebird was ”unknown” to science for so long. In 1992, researchers working near this site found the first nest of the species in Alaska—a hatched nest, with eggshells that helped identify it as that of a godwit. The first active nest of the subspecies was not documented until 2008, discovered by a U.S. Geological Survey crew conducting an inventory of breeding birds in nearby Aniakchak National Monument and Preserve. Around this same time, biologists at the Alaska Peninsula National Wildlife Refuge were also conducting systematic inventories across large portions of the Alaska Peninsula. Their work slowly painted a picture of the species’ range and habitat preferences in the region.

Dan Ruthrauff_Tibbitts points to MAGO nest
Researcher Lee Tibbitts points to a Marbled Godwit nest. Photo by Dan Ruthrauff.

These efforts culminated in 2006 and 2007 when Bob Gill, Lee Tibbitts, and I conducted systematic helicopter-based surveys to determine the breeding range of the subspecies in Alaska. Limited mostly to moist lowland meadows, the breeding range of the species in Alaska ranges from just south of Egegik Bay in the north to about Port Heiden in the south, a span of only about 150 km. Thus, the subspecies’ breeding range is small and remote and, curiously, is separated from the next nearest Marbled Godwit breeding location by about 2,500 km. We also trapped and equipped nine Marbled Godwits with solar-powered satellite transmitters; given the near-complete lack of information regarding the subspecies in general, we really did not know what to expect as these birds began their migratory movements.

To our pleasant surprise, we ended up tracking these birds for a long time; the last individual’s transmitter stopped functioning in October 2015. Not only did we learn a great deal about the basic migration ecology of this subspecies—much of which simply confirmed Dan and Brina’s original hypotheses based on deductive reasoning and critical thinking—but these migratory tracks also presented us with a unique opportunity to assess the degree to which individual Marbled Godwits were consistent in the timing of their migrations and their use of sites throughout their annual cycle.

Like many of their relatives, Marbled Godwits that breed in Alaska are homebodies, displaying a predictable attachment to a handful of sites. In contrast to globetrotting Bar-tailed and Hudsonian godwits, however, Alaska’s Marbled Godwits are highly flexible in the timing of their movements. It appears that the subspecies’ relatively short migration between its Alaskan breeding grounds and nonbreeding locations along the Pacific Coast of Washington, Oregon, and California affords these birds more opportunity to adjust the timing of their annual movements. The factors driving this flexibility ultimately remain a mystery—but this seems appropriate for a species that has hidden in plain sight for so long.

AUTHOR BLOG: Do Burrowing Owls aid in the long-distance dispersal of plague-infected fleas?

Kara Navock and Jim Belthoff

Linked paper: Investigation of the geographic origin of burrowing owl fleas with implications for the ecology of plague by K.A. Navock, D.H. Johnson, S. Evans, M.J. Kohn, and J.R. Belthoff, The Auk: Ornithological Advances 136:1, January 2019.

nestling
Collecting samples from a Burrowing Owl nestling. Photo by John Kelly, Boise State University.

Western Burrowing Owls (Athene cunicularia hypugaea) and Pulex irritans, the so-called human flea, have a curious host-parasite relationship. Although we’ve known about it for some time, many details of their connection remain unclear, including why it appears mainly in the northwestern portion of the Burrowing Owl’s range despite the fact that both species have much broader geographic distributions. We were interested in the potential interplay among the migratory movements of Burrowing Owls, the potential for dispersal of P. irritans through its affiliation with owls, and Yersinia pestis—the zoonotic (animal-transmitted) bacteria infamous for causing bubonic plague.

Outbreaks of plague continue to occur sporadically throughout western North America, and it is typically transmitted among susceptible rodent hosts via flea bites. Birds are generally thought to not be vulnerable to plague, but some researchers have suggested that birds of prey could move infected rodents between sites, thus contributing to the disease’s spread. We wondered if birds such as Burrowing Owls could instead be directly aiding dispersal of fleas, which could happen over much longer distances, perhaps even from plague-infected areas in the owls’ wintering range to their breeding grounds. Although P. irritans is not necessarily the key player in plague outbreaks in western North America, it is a possible vector, so a better understanding of the extent to which birds of prey facilitate its dispersal is important.

To help clarify the geographic origins of the fleas on Burrowing Owls, and therefore the potential for long-distance flea dispersal facilitated by migratory owls, we collected feathers, portions of toenails, and fleas from adults and nestlings in two breeding populations of owls in Idaho and Oregon. We then analyzed stable isotopes of hydrogen to decipher whether the fleas on owls had isotopic signatures reflective of owl breeding or wintering grounds. These isotope ratios vary predictably across the latitudinal gradient, providing a geographic map to help understand where our samples originated.

adult
An adult Burrowing Owl ready for sampling. Personal photo, Belthoff lab.

Our analysis was based on three assumptions: (1) adult owl feathers would show the isotopic signatures of the owls’ breeding grounds, because of the timing of feather growth, and (2) nestling toenails would have local breeding-ground hydrogen isotope ratios, but (3) adult toenails would reflect the isotope ratios of the owls’ wintering grounds, as toenails grow continuously and adults just arriving on the breeding grounds would have toenails recently grown in wintering areas. We reasoned that if the fleas we collected had hydrogen isotope ratios most like those of adult owl toenails, then they must have started out on the owls’ wintering grounds and hitched long-distance rides.

Assessing the hydrogen isotope ratios in over 250 fleas, we found that they were markedly different from the ratios in adult toenail samples, but they frequently matched those of the feathers and toenails of nestlings. This implies a breeding ground origin rather than a wintering ground origin for the fleas infesting the Burrowing Owls. Fleas from adult owls in the Idaho population however had a slightly more southern hydrogen isotope signature, which could mean that the owls were moving fleas over short distances, such as between recent migration stopovers and breeding grounds. However, we found no evidence of long-distance dispersal of fleas between the owls’ wintering and breeding grounds.

This lack of pronounced continent-level movement of fleas suggests that even during outbreaks of plague among wildlife, the chance of long-distance dispersal of fleas carrying plague bacteria is low, despite that Burrowing Owls in portions of their breeding grounds might be regularly “bugged” by P. irritans.

During completion of this research, Kara Navock was an undergraduate researcher participating in Boise State University’s REU Site in Raptor Research, funded by the National Science Foundation (REU Site Award; DBI 1263167 to JB) and Boise State University. In addition to authoring this manuscript, Kara was awarded a William C. Andersen Award for best student poster for her presentation at the 2017 annual meeting of the Raptor Research Foundation. As of January 2019, she is continuing her studies at Boise State University at the graduate level. Research into the ecology of Burrowing Owls and their host-parasite relationship with P. irritans continues in the Belthoff lab at Boise State University and through the Global Owl Project.