AUTHOR BLOG: Speciation with gene flow in Northern Saw-whet Owls

Jack Withrow

Linked paper: Speciation despite gene flow in two owls (Aegolius ssp.): Evidence from 2,517 ultraconserved element loci by K. Winker, T.C. Glenn, J. Withrow, S.G. Sealy, and B.C. Faircloth, The Auk: Ornithological Advances.

Dorsal and ventral views of specimens of the two Saw-whet Owl forms, showing plumage differences. Photos by Jack Withrow.

Scientists have long thought that for two related populations of birds to evolve into separate species, they needed to be completely separated. This usually means the kind of total separation produced by isolation on islands or by features such ice sheets, mountain ranges, or rivers. However, the complex distributions and migratory nature of many birds mean that long-term total separation of bird populations, long the assumption in speciation research, is actually not necessary for speciation to occur. As we’ve tried to better understand how bird populations diverge, other ways of explaining speciation have begun to receive more attention, and it’s becoming increasingly clear that speciation can happen even with low levels of gene flow. Learning how this can happen in migratory taxa has become an important focus in ornithology.

Northern Saw-whet Owls (Aegolius acadicus) occur across much of North America. A small, non-migratory population is isolated on the islands of Haida Gwaii in British Columbia (A. a. brooksi), and the nominate mainland form (A. a. acadicus) passes through these islands during migration but does not stop to breed. So, these two populations overlap during some parts of their annual cycle but not during others. Presently considered a subspecies, brooksi feeds heavily on intertidal invertebrates in winter and has strikingly dark plumage compared to the migratory form, acadicus. Although their geographic context suggests the potential for gene flow, no one has ever found any intergrades between the two populations, suggesting that ecological factors are playing a role in maintaining their separation. Reconstructing how these owls diverged is difficult, because we can’t know the exact history of the distributions and ecological contexts that preceded what we observe today in this glaciated region. However, genomic data can be used to test hypotheses about their divergence and tell us what the long-term demographic history has been.

Recent technological advances have vastly increased the amount of genetic data that can be generated to look at divergence in populations. However, it’s important to examine the same parts of a genome so that you are making apples-to-apples comparisons. Ultraconserved elements (UCEs) are sections of the geneome that are relatively easy to find and can be used to assess divergence at population to family and order levels. They provide a similar set of core sequences that increase in variability the further from the UCE you go, allowing the assessment of both deep and shallow divergences at the same place in the genome. We examined over 2,500 separate UCEs to infer the processes under which these data were most likely to have evolved, including population sizes, levels of gene flow, and time of divergence. We found that the model that best fit the data included an initial split between the two populations with a low level of ongoing but skewed gene flow: an average of about 0.7 individuals per generation coming from acadicus into brooksi, and about 4.4 individuals per generation going the opposite direction.

These results support our hypothesis that the divergence between these two forms included low levels of gene flow rather than complete isolation. The low levels of gene flow from nominate acadicus into brooksi, coupled with strong evidence of ecological selection, suggests that the Haida Gwaii owls are on an independent evolutionary trajectory. Nominate acadicus are not staying on Haida Gwaii and breeding with the islands’ owls with the frequency we might expect, and we believe that selection is operating differently on the two populations due to the fact that they focus on resources that are distributed differently in time and space. Despite the history of gene flow between the two populations, brooksi appear to be a young biological species.

AUTHOR BLOG: Getting to the bottom of male Black-throated Blue Warblers’ migratory behavior

Jessica Deakin

Linked paper: Sex differences in migratory restlessness behavior in a Nearctic–Neotropical songbird by J.E. Deakin, C.G. Guglielmo, and Y.E. Morbey, The Auk: Ornithological Advances.

A female and male Black-throated Blue Warbler in captivity. Photo by Jessica Deakin.

Many species of migrant songbirds have a reproductive strategy called protandry, where males arrive at stopovers and breeding sites earlier than females. Ornithologists believe that males do this because it increases their mating opportunities and reduces competition among males for high-quality nest sites. Although it’s a common phenomenon, the question of how males arrive earlier is still unanswered for most species. One thing we do know is that the difference in arrival timing between males and females appears to be similar across years, suggesting that the behaviors that contribute to protandry are innate.

For this study, we evaluated potential innate contributors to protandry in the Black-throated Blue Warbler (Setophaga caerulescens). Black-throated Blue Warblers are small songbirds that spend the summer in North America and the winter in the Caribbean, migrating at night. They have a lazy, buzzy-sounding song, and males are easy to distinguish from females — the males are a brilliant blue, while the females are olive-brown. We caught Black-throated Blue Warblers at a stopover site in southern Ontario, Canada, during their fall migration and kept them at Western University’s Advanced Facility for Avian Research over the winter.

During migration, caged birds display a behavior called migratory restlessness, which is characterized by extensive hopping and wing whirring (the fluttering of wings while perched) at night. The timing of this behavior’s onset in the spring corresponds with when the birds typically depart from their overwintering grounds, and the intensity corresponds with the duration of their migration. We used automated video analysis software to quantify the onset and intensity of hopping and wing whirring of our captive Black-throated Blue Warblers when spring arrived. We found that migratory restlessness began earlier in males than in females, suggesting that males have an innate disposition to depart for spring migration. Surprisingly, we also found that males displayed higher intensity wing-whirring behavior than females, suggesting that the sexes may have innate differences in flight behavior that could influence their migration rate.

A tagged Black-throated Blue Warbler after release. Photo by Sue Bishop.

Next, we outfitted our Black-throated Blue Warblers with digital nano radio-tags and released them where they were caught the previous fall. The tags let us use the Motus Wildlife Tracking System to determine when they departed from the stopover site, and we also used manual telemetry to monitor their behavior. The birds behaved normally upon release, foraging, preening, and singing, and they departed in a normal northern spring migration direction. This suggests that migratory birds readjust quickly to the wild after being held in captivity for several months — important information for wildlife rehabilitators.

Overall, this study demonstrated that males and females have different migratory restlessness behavior. We think males might make longer flights than females between stopovers. Our future studies will include looking at sex differences in flight characteristics, such as wing morphology and energy use during migratory flight.

AUTHOR BLOG: Are homebody warblers more likely to sing together?

Liam Mitchell

Linked paper: The evolution of vocal duets and migration in New World warblers (Parulidae) by L.R. Mitchell, L. Benedict, J. Cavar, N. Najar, D.M. Logue, The Auk: Ornithological Advances.

Family tree of duetting and migrating warbler species.

Scientists who want to study the evolution of behavior face a fundamental problem: unlike bones, behavior generally doesn’t fossilize. However, that doesn’t mean that extinct species’ behavior doesn’t leave any evidence. The behavior of living or “extant” species can give us clues about the behavior of their ancestors, and we can use the behavior of living species, the evolutionary relationships among species, and computational modelling to make inferences about extinct species’ behavior.

In our study, we used this approach to study the evolution of vocal duetting and migration in New World warblers. Vocal duetting is when a mated pair of birds sings together. Duets are a cooperative behavior, because they communicate that the duetting pair will cooperatively defend their shared territory against intruders. It’s hard for mated pairs to stay together through migration, so non-migratory birds tend to have longer-lasting pair bonds than migratory species. These longer pair bonds mean that non-migratory birds may have more to gain from cooperative behaviors like duetting, so we might expect duetting to be evolutionarily associated with the absence of migration. 

We tested whether migrating and duetting are correlated in the evolutionary history of New World warblers. Essentially, we were looking to see if duetting and the absence of migration show up in similar places on the birds’ family tree. We collected data on each warbler species and determined whether or not they performed duets and whether or not they migrated. We used these data to perform our analyses.

Our primary analysis generated an evolutionary tree that shows duetting and migration over evolutionary time. We borrowed an existing phylogenetic tree of New World Warblers (Lovette et al., 2010) and used a technique called Markov Chain Monte Carlo (MCMC) to simulate trait evolution (Revell, 2013). MCMCs are computer simulations that calculate the frequency at which a given node (a point where the tree branches) exhibits a specific characteristic over a number of simulated generations. The likelihood that a given generation exhibited a characteristic is informed by the other nodes on the tree, especially the nearby ones. The frequency with which a node exhibits a characteristic in the simulation can be interpreted as the probability that the ancestral species at that node exhibited the characteristic. For example, if we calculate one million simulations for the most ancestral node on the tree, and 800,000 of those simulations exhibit the characteristic “migration,” we can say there is a high likelihood (0.8) that the last common ancestor of all living warblers migrated.

This let us calculate the evolutionary correlation between duetting and migration. Our analysis showed that migration and duetting are indeed negatively correlated over evolutionary time. In other words, duetting is associated with a non-migratory lifestyle, as we predicted. These methods allow us to get a quantitative look at the evolution and loss of certain behaviors over time. We can then draw informed conclusions about the nature of these complex behaviors and open the way for studying the factors that may have influenced their changes over time.

Read more on the lab website.

AUTHOR BLOG: Fly like an eagle? Topography tells us how high Golden Eagles soar

Adam Duerr

Linked paper: Topographic drivers of flight altitude over large spatial and temporal scales by A.E. Duerr, T.A. Miller, L. Dunn, D.A. Bell, P.H. Bloom, R.N. Fisher, J.A. Tracey, and T.E. Katzner, The Auk: Ornithological Advances.

A Golden Eagle soars over a line of ridgetop wind turbines. Photo by Dave Brandes.

Like many people, I am fascinated by bird flight. Unlike most people, I get to study flight of Golden Eagles for a living. These large birds move through the landscape primarily by soaring—a style of flying where they hold their wings outward and rarely flap, saving them considerable energy. Instead of flapping, they rely on rising air currents to gain altitude.

Two types of rising air currents provide most lift for soaring eagles. The first, thermal updrafts, form when energy from the sun heats air at the Earth’s surface and causes it to rise. Eagles circle within these columns of rising air to gain great altitude and then glide out of the thermals to move across the landscape. The second, orographic updrafts, form when winds are deflected upward by structures such as ridges or hills. Eagles can then soar at relatively low altitude above and along these structures.

Although updraft formation depends on the interaction of weather and topography, our goal for this study was to determine if topography alone can explain how high eagles soar. To do this, we used telemetry systems that we placed on the backs of 91 Golden Eagles in California, which recorded the eagles’ locations every 15 minutes. For each of the almost 180,000 locations we recorded of eagles in flight, we compared the eagle’s altitude with the characteristics of the topography below.

We found a strong relationship between topography and flight altitude for the Golden Eagles in our study. In places where the topography made the formation of orographic updrafts likely, eagles were more likely to fly at lower altitudes, while in places where the topography made the formation of thermal updrafts likely, eagles were more likely to fly at higher altitudes. We also found that the effects of some topographic features depended on their region within California, which may be due to regional differences in weather patterns, land cover, or a variety of other factors that we did not include in our analysis. Our topography-based model of flight altitude is much simpler than other models of avian flight altitude, thanks to the fact that it lets us ignore weather conditions, which are constantly changing. Instead, we can simply estimate how high a Golden Eagle is likely to be flying as it crosses over any point of interest in California. Wildlife managers can use this type of information to predict where eagles may collide with wind turbines and power lines; therefore, making these predictions in an accurate and straightforward way is critical for Golden Eagle conservation.

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.