Towhee Trouble

Alright guys, you got me. I made a mistake on my last blogpost. When I described finding some brushfinches in the mountains outside Mexico City, I said "their phylogeny is quite interesting, but maybe I'll save that topic for another blog post," and you smug bastards were on to me immediately. Against overwhelming pressure from my readers and haters, I have no choice. I admit it. I was referring to Charles Sibley's classic 1950s research on the hybrid zone between Collared and Spotted Towhees in central Mexico, and I absentmindedly thought it was a paper about brushfinches. I don't think I ever actually read the paper, I think I must have just seen it discussed somewhere. I had the image of the brushfinch-like Collared Towhee in my head and got mixed up. No one is perfect and I'm admitting my mistake, so please, take it easy with the death threats and hate mail. My inbox is overflowing!

In any event, I'd like to wipe the slate clean and dig into this research a little bit. Charles Sibley's work is blogpost-worthy for several reasons. Firstly, I get a kick out of reading these classic research papers from decades ago, and I hope you will too. Gone are the days when a biologist could go swashbuckling into Mexico with nothing but a small team of student assistants, and collect samples across the entire latitudinal gradient of the country. Sibley's paper contains a tinge of the old adventure writing style that one might find in naturalist narratives for instance from Darwin, or Bartram's Travels. 

Another amusing quirk of science writing from this time is that you can find prominent researchers with polar opposite views on now well-established subjects. Moreover, they were not afraid to express their extreme opinions with hostile confidence. In his introduction, Sibley illustrates how controversial the subject of hybridization was at the time by first quoting Edgar Anderson's view that "introgressive hybridization is certainly more important than all other factors combined in providing raw materials for natural selection to work upon," and immediately follows this with G. Ledyard Stebbins' view that "introgressive hybridization, whatever may be its importance in modifying and amplifying the variation pattern of certain individual species, is nevertheless by its very nature not a way of producing new morphological or physiological characteristics, and therefore of progressive evolution." Science is simply more fun when you have one researcher who's certain that hybridization is the most important factor by far in evolution, while another believes it isn't a factor at all. Nowadays, we know much more about this subject, and these types of arguments tend to quickly fizzle out into a middle-of-the-road "it depends." 

Getting to the meat of the paper, Sibley took on the unique and troubling case of a hybrid zone between two bird species in Mexico: the Collared and Spotted Towhee. Hybrid zones can take on many forms and result from many different situations, but one textbook process that is a useful baseline example is as follows: one freely breeding population gets bisected, possibly by some geographic change such as a river or mountain formation, and reproductive isolation ensues. Over time, the two populations diverge genetically, and eventually, through range shifts/expansion, come into "secondary contact" with each other. At this point, genetic incompatibilities have built up during their isolation, but perhaps not enough for them to consistently recognize each other as different. They interbreed, but because of these genetic differences their hybrids are inviable or less fit for any number of reasons. Total reproductive isolation is rarely achieved in nature, but if hybrids have lower fitness, various mechanisms may discourage interbreeding, and the hybrid zone will gradually grow smaller and less relevant. The exceptions to this, where stable hybrid zones are maintained instead of diminished, often end up being more nuanced and interesting. In some cases, hybrids form fairly stable and recognizable types, think for instance of Brewster's and Lawrence's Warblers, or hybrids between red-shafted and yellow-shafted Norther Flickers that end up with predictable intergrade orange shafts. What makes Collared and Spotted Towhee hybrids so unique and challenging is that they exhibit less predictable variation across several traits (Sibley identifies six key traits that vary between species), and hybrids are far-flung across a range of hundreds of miles. 

Broadly speaking, the pure-blooded Collared Towhees are in western Mexico, and moving east one begins to find specimens with more black on their cheeks and throats. Eventually, their distinctive white supercilium disappears altogether as it is filled in with black. Moving even further into the center of this range, the classic Spotted Towhee rufous flanks begin to show up. The olive green back remnant of Collared Towhees doesn't disappear in specimens until one reaches all the way over very nearly to the eastern coast (DeRaad et al. 2023, a paper I will be discussing shortly, has some terrific graphics that illustrate these various types). This is a bit of an oversimplification however, as across this range researchers found a huge amount of variability, and Sibley identifies several different clines operating at once. Despite these complications, Sibley writes that there's no doubt that this pattern of variation resulted from hybridization between two distinct species. But where did the hybrid border initially form? Why are introgressed traits so wide ranging in this case? Are the different plumage characteristics adaptive in some way? What are the implications of these results for the role of hybridization in evolution writ large? These questions Sibley offers some initial thoughts on, but for the most part he leaves them standing as a challenge to simplistic and idealized conceptualizations of the species question.  

This is a perfectly reasonable conclusion to leave us with, especially given the relatively limited tools Sibley had at his disposal. The truly astounding follow-up however, is that researchers reevaluated Sibley's hybrid zone in 2023, marshalling all the modern genetic resources available to them to answer these questions, and they still wound up short. DeRaad et al. were able to dismiss one of Sibley's hypotheses that recent human-made habitat alterations had caused the unusual hybrid distribution by showing that in the 70 years since Sibley collected his specimens, the genetic picture remained largely the same. This finding displays more stability in towhee hybrid forms than would be expected of a recently formed hybrid zone, and lends more credence to the theory that a longer time frame of hybridization caused the resulting variation. DeRaad et al. postulated that secondary contact may have occurred more than one thousand years ago. DeRaad cleans up a few of Sibley's other misapprehensions and provides a wealth of new genetic context to the picture, but ultimately finds that these towhees are pretty much just as tricky today as they were 75 years ago. 

DeRaad et al.'s results confirm that Collared and Spotted Towhees do not form a typical "tension zone," where two distinct species' ranges meet in the middle and suffer from low hybrid fitness. The hybrids are too wide ranging and have "erased nearly all fixed autosomal differences between the two ends of the cline" (DeRaad et al. 2023). They also consider the possibility that the range represents a complex of multiple semi-isolated lineages of towhees that are in the process of developing reproductive isolation, and potentially even full species status, but yet again come up short of anything conclusive. It is possible that hybrids are hybridizing with other hybrids, creating novel variation and complicating the picture even further! DeRaad painstakingly characterizes the individual trait variation and provides compelling evidence of how various traits could be adaptive in different parts of the complex patchwork of habitat, but since many traits seem to vary individually and sometimes along different gradients from other traits, it is quite difficult to explain in total. Researchers find several candidate regions where more genetic differentiation exists between populations, but never enough to confidently establish species or even subspecies delineations. 

No doubt somewhat exasperated, DeRaad et al. conclude "it is humbling to recognize that many of the novel genomic patterns we document here bear out Sibley's (1950) taxonomic recommendations." The unique biogeography of their range, and the complex and thorny patchwork of their hybrid interactions bely simple categorization, even after 75 years of study. Echoing the sentiments of a paper I covered in this blogpost, modern genetic methods, as comprehensive as they've become, do not always offer easy solutions to nature's pesky idiosyncrasies. From purely phenotypic work done 75 years ago up to the modern genomic techniques of today, the specific nature of this species relationship remain hidden away, locked in mystery, like Excalibur locked in stone. Will there ever be a hero strong enough to pull out the truth? 

Bibliography:

Sibley, Charles G. “Hybridization in the red-eyed towhees of Mexico.” Evolution (1954), vol. 8, no. 3.

DeRaad, Devon A. et al. “Hybrid zone or hybrid lineage: a genomic reevaluation of Sibley's classic species conundrum in Pipilo towhees.” Evolution; international journal of organic evolution (2022): n. pag.