Infus'd Betwixt Part 3: The Protean Paruline

Yellow-rumped Warbler (Setophaga coronata)

Photo: Alan D. Wilson (Wikimedia Commons)

This is the final part of a three part series on hybridization in warblers (family Parulidae) called Infus'd Betwixt.

Earlier in this series of essays, I looked at two situations where hybridization is widespread and leading to a diminution of biodiversity; one of those cases is a human-induced process and has just begun in the last century or so, while the other appears to be a millennia-old natural process. It's a fact of life, as it were, that hybridization can cause the loss of species; it can also lead to the creation of species. Hybrid speciation has long been recognized in plants, but not until recently has it been shown to play a similar role in the production of animal diversity. The hybrid origins of a number of bird species has been proposed but molecular evidence to corroborate such suspicions has been equivocal or altogether lacking. The Yellow-rumped Warbler (Setophaga coronata) is the first example of hybrid speciation in birds.

Before we get too far along I’ve got to tell you that Yellow-rumped Warbler taxonomy is, like so much in the biological sciences, far from simple. Most North American ornithologists recognize four distinct subspecies, not full species, of Yellow-rumped Warbler. Each of these subspecies differs from one another mainly in their head and face plumage. The protean subspecies are the nominate coronata which occurs throughout the boreal forest; auduboni, mainly west of the Rocky Mountains; nigrifrons in Mexico’s western Sierra Nevada; and goldmani in Guatemala. That’s the view of the American Ornithologists’ Union (AOU), the big boss man of North American bird taxonomy. By contrast, the International Ornithological Congress (IOC), which has limited influence over the goings on of North American ornithology, considers coronata, auduboni, nigrifrons and goldmani to be four distinct species.

This taxonomic controversy is nothing new. Each of the four distinctive subspecies (I’ll stick with the AOU definition), were originally described as a separate species: coronata by Linnaeus in 1766, auduboni by Townsend in 1837, nigrifrons by Brewster in 1889 and goldmani by Nelson in 1897. Eventually, owing to the similarities in their plumages nigrifrons and goldmani were lumped as subspecies of auduboni. That meant that by the 1920’s only two species remained: coronata and auduboni. However when it was discovered that the two remaining species hybridized, they too were lumped to form one species with four rather distinctive subspecies. Even with the solid molecular data available today, the current taxonomic disagreement between the AOU and the IOC has not had a final resolution.

Let's not get bogged down in the Yellow-rumped Warbler species/subspecies debate. Just bear in mind that the process of by which subspecies arise is more or less the same as the process by which full species arise, it's just a matter of degrees. Speciation can lead to fully formed species, with enough genetic distance from their congeners to be considered something onto themselves, or it can mean the evolution of incipient, but not yet full species. Incipient species are ones that aren’t quite there yet, they’re not genetically or phenotypically distinct enough to stand alone, to avoid hybridization, to count as fully-formed, honest-to-goodness species. Full or incipient species status for the Yellow-rumped Warblers doesn’t make too much difference in terms of our discussion. The process of hybrid speciation is the same, as I've said, it’s just a matter of degrees. Because evolution is such a gradual process all species begin as incipient species, before becoming a full species species. Regardless of whether you take the AOU or the IOC view, the Yellow-rumped Warblers still present us with a fascinating and important biological story and, unlike all the other putative instances of avian hybrid speciation, this one is supported by genetic data.

So just what does that molecular data say? It shows that coronata and auduboni are closely related, their mtDNA differing by only by about 0.2% (a minuscule difference), and that they hybridize often when they occur in sympatry. These are the reasons that the AOU considers the Yellow-rumped Warblers to be subspecies and not full species. The data also shows that coronata and auduboni DNA differs greatly from nigrifrons and goldmani and that the later two subspecies split from the former two about 1.7 million years ago. The molecular data also suggests that auduboni, had a rather remarkable origin.

Auduboni has within its DNA some genes of both coronata and nigrifrons. There are some visual clues too: auduboni resembles nigrifrons, both posses a yellow throat, a bold white patch on the wing, an indistinct eyeline and a fairly dark face. Morphometrically, northern populations of auduboni are intermediate between coronata and nigrifrons. In the southern part of the Audubon’s range, birds are morphometrically most similar to nigrifrons.

Perhaps the most telling clue to auduboni’s hybrid origins are something called private alleles. Private alleles are forms of genes found only within one species. They’re found solely there and nowhere else because they arose through evolution in that species alone. A species with an evolutionary past that involves hybridization would share some alleles, or forms of DNA, with its parent species. It may evolve some of its own private alleles but it will certainly have genetic material that is shared by its parent species. In the case of auduboni, almost all of its DNA and mtDNA is shared with coronata and nigrifrons. There are only a small number of auduboni-specific alleles, which are recently evolved and unique to that subspecies. By contrast, almost no alleles are shared by coronata and nigrifrons except for one, which is probably an ancestral allele left over from a deeper evolutionary time when all the subspecies had yet to split from a common ancestor. The abundance of shared alleles suggests that auduboni may be have a hybrid origin, with coronata and nigrifrons being the parent subspecies.

Is it not possible that nigrifrons could have arisen through regular old speciation - that is to say, without hybridization? When we look closely at the DNA it appears that simply cannot be the case. If all three of these subspecies came from a common ancestor in the recent past it stands to reason that they should all carry some similar alleles. So if the origin of auduboni was through the normal speciation process, then private alleles should be equally common among all three subspecies. As I’ve said, that’s not the case.

It’s difficult to say where or when this hybrid origin occurred. Presently there are two known Yellow-rumped Warbler hybrid zones. One is an active coronata × auduboni hybrid zone spanning a 150 km wide swath of western Alberta and British Columbia (which incidentally includes the aforementioned Peace Country). Further south in Arizona, auduboni × nigrifrons hybrids have been discovered. But there is currently no hybrid zone between coronata and nigrifrons pumping out auduboni. When this might have occurred remains uncertain, but it was certainly sometime in the very recent past, maybe even as recently as 16 000 years ago. The scenario that some ornithologists propose is that auduboni may have arisen at the end of one of the last glacial maxima, when the previously allopatric coronata and nigrifrons came into contact and began interbreeding. After it had been isolated from its parent subspecies in another glacial refugium during a subsequent ice age, auduboni spread outward across western North America when post-glacial conditions allowed. It’s been proposed that the initial hybridization between coronata and nigrifrons took place in the Canadian Rockies, just as with so many other species pairs; indeed auduboni and coronata form hybrid zones there today. Perhaps genetic technology and prehistoric climate modelling will eventually give us a better picture of the way in which all the warbler species and subspecies arose.

Infus'd Betwixt Part 2: When Two Become One

Black-throated Green Warbler (Setophaga virens)

Illustration: Louis Agassiz Fuertes (Wikimedia Commons)

This is part two of a three part series on hybridization in warblers (family Parulidae) called Infus'd Betwixt.

Humans have a knack for screwing up nature (needless to say). We’ve occupied almost every patch of productive habitat on the planet. We’ve not only occupied them, we’ve altered them too. One of the more obscure aspects of habitat alteration or outright destruction is the diminishment of isolating barriers that cause allopatric speciation. We don’t talk about habitat destruction in this way very often, but it has some grave consequences for certain species. Because humans are causing the ever more rapid destruction of geographic barriers between species, hybridization may very well be emerging as a more common phenomenon. Human-induced hybridization is yet another startling way in which we are managing to rid the Earth of its biodiversity. Golden-winged and Blue-winged Warblers in eastern North America seem to be falling victim to this kind of human-induced hybridization.

Determining the exact historical distribution of Golden-winged and Blue-winged Warblers is impossible but the notes left by 18th and 19th century ornithologists suggest that these two species occupied distinct ranges. They were mostly allopatric; Golden-winged Warblers to the north, Blue-winged Warblers to the south (with a little overlap here and there). By the late 1800’s a significant chunk of America’s eastern primeval forest had fallen to the axe. In its place were the indelible marks of human progress: pastures, fields, shublands and thickets. For millennia, dark and brooding forest which both species shunned in favour of more open habitats kept the breeding ranges of Golden-winged and Blue-winged warblers discrete. Each species followed their respective evolutionary trajectories with almost no chance to interact, almost no chance to interbreed. It was allopatric speciation at work and the forest separating the two species was crucial to seeing the process through to its end.

But as the axe and saw tore the forest barrier down, the Blue-winged Warbler began expanding its range into that of the Golden-winged Warbler. In many cases the Blue-wings occupied exactly the same habitats used by the Golden-wings: early successional shrubby habitats with adjacent forest edges. The scientific literature suggests that Golden-wings prefer slightly wetter habitats than their congeners, while Blue-wings prefer habitats that are slightly older and more ingrown. But these distinctions are not concrete and in many places both species occur in exactly the same habitat. Without the benefit of habitat differences to keep the species apart, the Blue-winged invasion was swift and not without consequences. In some places it took only a half century for Golden-winged Warblers to disappear, being replaced by their congener. Some areas have seen long periods of continued coexistence between the two species, but in general, following invasion by Blue-wings, the Golden-wings disappeared.

The decline of the Golden-winged Warblers continues at a rate of 15-18% annually throughout (most of) the remaining part of their range. Though not yet federally recognized as a species at risk in the United States, it is listed in Canada as threatened. The Golden-winged Warbler’s decline clearly has something to do with the Blue-winged Warbler, but what exactly? Was it the result of competitive exclusion of Golden-wings by more aggressive Blue-wings? It seems that in some interactions Blue-winged Warblers are the more aggressive species, but that isn’t always the case; some researchers have actually found that the Golden-winged Warbler to be the dominant species. In some parts of their shared range they respond to each others’ songs in aggressive ways. In others areas they don’t appear to consider each other competitors and overlap their territories without conflict. The dynamics of interspecific interactions during ecological invasions of this kind are complex, especially when invasions happen over a fairly large area. It can be hard to determine what leads to one species success at the expense of another. There has yet to be put forward a good explanation as to why the Blue-winged Warbler is managing so well, while the Golden-winged is in such dire straits. Understanding the interactions between these species becomes even more daunting when you consider they hybridize with impunity.

Wilson never saw a hybrid. Neither did Audubon. Neither did their contemporaries. The first Golden-winged × Blue-winged hybrid (a Brewster’s Warbler) wasn't discovered until 1874. The Brewster’s Warbler was a new thing in the late nineteenth century, and perhaps the first example in North America two species making contact across a geographical barrier because of human meddling. It marked a major milestone in the evolution of the Golden-winged Warbler; a milestone which may prove to be the last one on the Golden-wing's road.

Under normal circumstances hybrids are rare in nature, but in places where Golden-wings and Blue-wings co-occur, you can usually find hybrids flitting about without too much trouble. That’s a sure sign that interbreeding is happening often, perhaps more often than the casual observer realizes. While sometimes hybrids are obvious, other times they are not. That’s because a bird's outward appearance is not necessarily a true reflection of its genes. It takes some molecular detective work to diagnose some hybrids, thus the true extent of hybridization between Vermivora, one might say, is often hidden in plain sight.

Hybridization between Golden-wings and Blue-wings is so extensive that collectively the species have been called a hybrid swarm. A hybrid swarm describes a situation where members of a mixed-species population posses genes from other species, in addition to their own, as a result of hybridization and backcrossing. This means that if you take a Golden-wing from anywhere across its range and look at its genes you will find Golden-winged genes, but you will also find Blue-winged Warbler genes mixed in there too. Even birds that outwardly appear to be pure – they show no aberrant plumage – may very well be genetically impure. You may have a pair of Golden-winged Warblers breeding among the Northern Prickly-Ash (Zanthoxylum americanum) in your back forty, as I do. There may be no sign of Blue-winged Warblers in the area. That doesn’t mean your Golden-wings are pure. They could very well be carrying genetic material from both species. How did they get those Blue-wing genes if there are no Blue-winged Warblers around? The most likely explanation is that they were carried there by dispersing birds. Even a single impure Golden-wing, with origins from a place where hybridization is rampant, settling and successfully breeding on your farm is all it would take to pollute your local Golden-wings. The bottom line is that the only way to tell how genetically pure any bird is involves looking at its DNA.

Is anywhere safe from genetic mixing? There's some evidence that Manitoba and Quebec may harbour hybrid-free populations. Recent sightings of Brewster’s and Blue-winged Warblers in Manitoba means that the birds in that province are likely to start becoming polluted with Blue-winged Warbler genes. Until recently the relatively isolated Manitoba population remained out of reach of dispersing hybrids or Blue-winged Warblers. It was a safe haven for those precious pure Golden-wing genes. But how much longer that will last, who knows? Refuges of pure Golden-winged Warblers may exist elsewhere. Certainly not all Golden-winged Warblers in areas of sympatry show signs of hybridization; a 2009 study found less than 18% of the birds they sampled in some parts of the species’ range had polluted genes.

The pattern of gene flow between the two species is bidirectional, so typically-plumaged Blue-winged Warblers across their range (except in Kentucky, for some undetermined reason), have Golden-winged mtDNA. In exactly the same way that the Golden-winged Warbler’s genome is being polluted by the Blue-winged Warbler, the Blue-winged Warbler’s genome is being polluted by the Golden-winged Warbler. An eye for an eye. Or rather, a black-throat patch for a white one. If it’s genetic mixing we’re worried about, than the Blue-winged Warbler is at as much risk as the Golden-winged Warbler, but it doesn’t seem to get the same amount of attention.

One reason is probably because Blue-winged Warbler numbers are on the increase, and their range is expanding, while Golden-winged Warblers are suffering rapid declines with 64% of the global population of Golden-wings lost since the 1960’s. That’s speaking phenotypically of course. Are genetically pure Blue-winged Warblers actually on the increase? Early studies of the genetic interactions between Golden-wings and Blue-wings showed that gene flow was asymmetrical so that while Golden-wing genes became polluted, Blue-wing genomes remained relatively pure. We now know that’s not the case – gene flow is bidirectional. The genetic mixing flows both ways, leaving little chance genetically pure Blue-winged Warblers are faring much better than genetically pure Golden-wings.

The Vermivora situation is not the only one that has arisen due to human-caused environmental change. Another example can be found in a beautiful region of western Canada called the Peace Country. The Peace Country is a remarkable place because it’s the interphase of eastern and western flora and fauna. It’s here that species typically found west of the continental divide spill over the Rocky Mountain’s spine, mingling with eastern species they wouldn’t normally encounter elsewhere in their range. Pairs of closely related eastern and western warblers come into sympatry in the Peace Country, and that means that conditions are ripe for hybridization. Black-throated Green Warblers (Setophaga virens) meet Townsend’s Warblers (Setophaga townsendi). They hybridize. Myrtle Yellow-rumped Warblers (Setophaga coronata) meet Audubon’s Yellow-rumped Warblers. They hybridize too. Mourning Warblers meet MacGillivray’s Warblers (Geothlypis tolmiei). They also hybridize; and in their case it’s a relatively new fling, still fresh and passionate.

The Mourning × MacGillivray’s hybrid zone appears to be relatively new one. Mourning Warblers were apparently absent from northeastern British Columbia in the early part of the 1900’s. The first reports of this species came in the 1970’s. It was no accident, Mourning Warblers had some help accessing the Peace Country. Like the Vermivora warblers, Mourning and MacGillivray’s Warblers love shrubby open habitats, and shun the deep dark woods. Early regeneration of clear cut logging sites provides ideal habitats for these species. It was probably through range expansion into clear cut areas that Mourning Warbler reached the Peace County and came into contact with their closest relatives, MacGillvray’s Warbler. Human enterprise once again leads to the removal of a critical geographic barrier to hybridization, and biodiversity suffers.

There was a long running debate whether these two species actually hybridized. Apparent natural variation of traits within each species had led some biologists to doubt that birds which showed intermediate or mismatched phenotypic characteristics were hybrids. The best phenotypic trait for distinguishing the species is prominent white eye arcs in MacGillivary’s. Mournings are usually without eye arcs, but occasional birds throughout the species range may have narrow ones. Are these hybrids that have dispersed out of the hybrid zone? I’m not sure anyone can answer that. Immature birds can be really difficult to distinguish, even using formulae that take into account the relative length of tail and wing, an often reliable measurement for separating genetically pure adult Mourning and MacGillvray’s Warblers. So this situation was already complex long before the hybrid zone was confirmed using molecular techniques.

Hybridization and genetic mixing between Mourning and MacGillvray’s Warblers is really quite different from the Vermivora warblers. In this case the hybrid zone is estimated to be only about 130 km wide, and there’s little evidence to suggest that the genetic mixing generated there extends out into the wider range of both species. This is in sharp contrast to the Vermivora which hybridize across their highly overlapping ranges. It’s hard to say what keeps that hybrid zone so narrow.

East of the Rocky Mountains you'll find Morning Warbler, west MacGillvray’s Warbler. Generally speaking, you can recognize them by looking at their mtDNA or their Z chromosomes (analogous to the X chromosome in humans). Or for the more field-oriented naturalist, you may examine their plumage. Birds living east of the Rockies don’t have bold eye rings – the most important field mark for distinguishing these two species – west of the Rockies they’ve got more pronounced eye rings. The pattern also holds for song. Birds in the east have a song that is more or less distinctive from birds in the west, though it can require a little practice to tell them apart.

The seemingly convenient genetic and phenotypic separation of species falls apart within the hybrid zone. Genetic traits become mixed together, so that individual birds cannot be assigned to one or the other species based on their mtDNA or Z chromosome markers. There is a mix of complete, partial and absent eye arcs, and vocalizations become weird admixtures of Mourning and MacGillvray’s songs. Within the narrow hybrid zone it’s pretty much impossible to reliably identify pure birds and hybrids by plumage or song alone. The use of molecular techniques in combination with plumage characteristics could be the best way to pick out which birds are hybrids and which birds are not. Sometimes biology is far messier than field guides would lead us to believe.

Why don’t hybrids and backcrosses spread their mixed-species genes into the ranges of their genetically pure parent species? Are there evolutionary forces selecting against hybrids? No one is sure when it comes to Mourning and MacGillvray’s Warblers. But they are not the only ones in the Peace Country with a narrow and seemingly newly established hybrid zone.

Before the discovery of the Peace Country hybrid zone, only one putative Black-throated Green × Townsend’s Warbler hybrid was known. To look at its plumage any ornithologist would have called it a classic Townsend’s; genetically though, the story was different. It had the mtDNA of a Black-throated Green Warbler. At that time the two species were thought to have completely allopatric distributions, but given their plumage, song and behavioural similarities, as well as their recent divergence (about 1 million years ago or less), it was perhaps not surprising that these two species could interbreed if they ever came into contact.

Like Mourning Warbler, Black-throated Green Warbler may be new to British Columbia. The first bird was collected only in 1965. Since that time they have become locally common in some eastern parts of the province, including in the Peace Country where it forms a hybrid zone with its western counterpart, Townsend’s Warbler. It’s a narrow zone, seemingly only about 40 km wide on the east side of the Rocky Mountain crest. Similar to the Geothlypis warblers, Black-throated Greens east of the Peace County are distinctive from west-side Townsend’s. They differ in genetics, plumage and song. But in the contact zone there are individuals that sport intermediate genes and plumage, they’re fairly rare, but they’re there. Some birds in the contact zone can switch between the songs of both species and both species respond aggressively to the other’s vocalizations. Whether this is another sign of hybridization or simply just learning the wrong specie’s song is still an unanswered question. Also, many hybrid zone birds are intermediate for traits such as wing length, tail length and beak width. On average, birds in the allopatric populations would be separable based on such morphometrics.

Ornithologists have some reason to believe that the narrowness of the Black-throated Green × Townsend’s Warbler hybrid zone might be maintained by natural selection eliminating hybrids because their intermediate characteristics make them unfit. A number of things may be at work here, including that hybrids might have a disadvantage when it comes to migration and life on their wintering areas. Both species have very different migratory routes and distinct nonbreeding habitats. If hybrids have inherited a mixed bag of traits from their parent species they may be quickly weeded out of the population by taking an unsuitable route on migration or by attempting to winter in poor habitat. Inheriting maladaptive traits might be keeping the hybrid zone narrow. In the case of Vermivora hybrids, there apparently hasn’t been strong selection against them, so perhaps that's one reason why their hybrid zone has expanded. These two scenarios, narrow and broad hybrid zones, show that evolutionary history, geography and a little serendipity are all important in establishing patterns of hybridization among warblers. But the hybrid story doesn’t end there. At the other end of the Townsend’s Warbler’s range there’s something else going on. Something different and fascinating and worrying.

Townsend’s Warbler and Hermit Warbler (Setophaga occidentalis) diverged within the past 500,000 years. Diverged yes, but differentiated, hardly. By that I mean, although they took on different plumage characteristics in allopatry, their ecology and life history strategies remained almost identical. They’re so similar in fact, that when these species do coexist in the same patch of forest they maintain territories from which they exclude not only their cospecifics but from each other. They sing very similar or identical songs. They share similar breeding phenology and habitat preferences. And they hybridize.

Townsend’s and Hermit Warblers meet in the three distinct hybrid zones in the Olympic and Cascade Mountains of the Pacific northwest. Hybrids are more common than pure Townsend's or Hermits in Washington’s Olympic Mountains, occurring at a frequency of over 60%. In the Washington Cascades about 43% are hybrids and in the Oregon Cascades about 28% are hybrids. Why the difference? And is this difference meaningful in any biological way? It is unlikely that there are sufficiently different selection pressures at each of the three hybrid zones which can account for the differing proportions of hybrids in each respective location. For example there are no apparent differences between the vegetation in territories of Townsend’s, Hermits and hybrids across the three sites. No other ecological differences have been detected either. Hybrids must be rarer the further south you look for another reason.

The greater frequency of hybrids in the Cascades is probably the result of dispersal of Townsend’s Warblers out of the Rocky Mountains. By contrast, the more isolated Olympics, have received an almost total lack of Townsend’s Warbler immigration from the Rockies, thus resulting in fewer hybrids and more genetically pure Hermit Warblers. Genetic data bear out this hypothesis. The influence of an excessive influx of pure Townsend’s Warblers into the Washington Cascades can be seen in the genomes of birds in the contact zone. This is not the case in the Olympics. There are plenty of forested corridors with suitable Douglas-Fir (Pseudotsuga menziesii) habitat for Townsend’s Warblers to disperse between the Rockies and the Washington Cascades. The apparent level of dispersal between the Washington and Oregon Cascade hybrid zones is far lower and lower still is dispersal into the Olympics. At least among the Cascade hybrid zones, the discordance between the frequencies of hybrids in the three zones may also be linked to the age of the contact zone. The Washington Cascades zone has probably been in existence for at least several thousand years. The Oregon zone, is estimated to be far younger.

But the three hybrid zones we see today are not the same ones that have always existed. The present day hybrid zones have shifted south by about 2000 km from the site of initial contact between Townsend’s and Hermit Warblers, somewhere in British Columbia. Indeed Townsend’s Warbler has replaced Hermit Warbler over this vast swath of the Pacific Northwest. The displacement of Hermit Warbler was partly through the usual ecological processes of competitive exclusion, where the behaviourally dominant Townsend’s Warbler ousted the subordinate Hermit Warbler, but also involved a significant amount of hybridization. The hybridization left what researchers have termed a "wake" of Hermit Warbler mtDNA in the Townsend’s warblers that today occupy this zone.

These two species have such broad ecological overlap that they could occupy the exact same habitats if and when they co-occur. Nature however, has a way of sorting communities of organisms so that very often only a single species is able to occupy a particular niche or habitat, to the exclusion of all other similar species. In the case of our two warblers, there is an unevenness in competitive ability with Townsend’s Warbler males being more aggressive than Hermit Warbler males. When these species to come together, Townsend’s Warblers bully and harass Hermit Warblers. Overtime, Townsend’s Warblers outcompete and push out their congener counterparts. The Townsend’s Warbler’s competitive superiority doesn’t end there. Townsend’s Warblers seem to be more successful at attracting mates, of both their own species and Hermit Warblers. It’s a dreary state of affairs for Hermit Warblers when these two species meet.

It has been suggested that the hyper-aggressiveness of Townsend’s Warbler may be a result of its recent evolutionary past. Although fairly large at present, the breeding range of Townsend’s Warblers may have been severely reduced during the last glacial maximum, when it was confined to a relatively small and arid refugia in the continent’s interior. The restricted and stressful conditions there probably led to extreme competition for limited territories in this highly restrictive habitat. In such a scenario, only the most aggressive birds would establish territories and produce offspring, and hyper-aggressiveness would be selected for. The ice age breeding range of Hermit Warbler was more expansive, so perhaps competition would have been less intense in that species.

Aggressiveness in birds is influenced by a number of bio-chemical (and other) factors. Testosterone and other androgens play an important role when it comes to territorial defense. Androgens levels are highest in Townsend’s Warbler males. Hybrids males are next, with significantly higher androgen levels than pure Hermit males. It appears that differences in androgen levels may be inherited. It’s been found that hybrids which are phenotypically more Townsend’s-like have higher androgen levels than hybrids that are more Hermit-like.
In short, Townsend’s Warbler appears to be the better species. Star Trek enthusiasts may think of Townsend’s Warblers as an avian Khan, superior in every way to the feeble and passive Hermit Warblers. Compared to Hermit Warbler, in marginal habitat, Townsend’s Warbler is able to achieve better pairing success and is better able to maintain their territories, even in resource-stressed conditions. Townsend’s usurp male Hermit territories and produce fertile hybrid offspring after mating with Hermit females. Hermit Warbler’s even lose out to hybrids, which have better pairing success and maintain their territories more effectively than pure Hermits. But, Townsend’s warblers still maintain their place at the top; they have larger clutch sizes and greater reproductive success than hybrids.

Contained within the genome of Townsend’s Warblers are haplotypes which signal a rapid demographic expansion following a period of population bottleneck. That bottleneck, a period where the population was low and mating options were limited, probably occurred in the Townsend’s Warbler’s glacial refugium. With the receding of the glaciers the Townsend’s Warbler rapidly expanded, eventually moving into the range of the Hermit Warbler. Townsend’s Warblers that inhabit the Pacific coast rainforests are the product of hybridization, as they carry over 50% Hermit Warbler mtDNA. As coastal Townsend’s Warblers moved south they initiated further hybridization with Hermit Warblers. They also continued to push the Hermits out of previously occupied habitat. The result is that there may very well be a natural extinction in progress. Some researchers estimate that genetically pure Hermit Warblers may have a mere 5000 years left before being completely swamped by the behaviourally dominant Townsend’s Warbler. The remaining birds will look like Townsend’s Warblers, but coast populations will continue to maintain a signature of past introgression with Hermit Warblers.

In Part 3 of Infus'd Betwixt, I'll look hybridization from another angle, how it can lead to speciation in birds.

Infus'd Betwixt Part 1: Hybridization in Warblers

Blue-winged Warbler (Vermivora cyanoptera).

Photo: Mark Conboy

I like hybrids. It's an atypical interest, I know, but maybe it has something to do with the fact that hybrids are for all intents and purposes, freaks of nature, and we all, in our own strange and twisted ways can’t get enough of freaks.

Nature has gone to great lengths to ensure that hybrids are rare, to ensure that like breeds with like and that like produces like. That Yellow Warblers (Setophaga petechia) breed with Yellow Warblers and give rise to more Yellow Warblers, that Pacific Giant Octopi (Enteroctopus dofleini) breed with Pacific Giant Octopi and give rise to more Pacific Giant Octopi, that Elm Sawflies (Cimbex americana) breed with only with Elm Sawflies and...you get the idea. That’s the normal course of things: when two individuals hook up, they normally chose members of the same species with which to do the dirty deed. Sometimes though, things don’t go as they should, and from time to time, members of two distinct species will mate and produce offspring – they hybridize.

Over time, differentiation between species has resulted in the development of barriers to hybridization, and it’s those barriers which keep each species on an independent evolutionary trajectory. These barriers can take various forms, but in essence each serves to make it impossible or at the very least difficult, to hybridize.

The most obvious kinds of barriers to hybridization are the phenotypic ones: to look, sound, smell or taste different from other species. Then there are genotypic barriers such as genetic incompatibility. This means that even if two heterospecifics (two individuals of different species) mate, their gametes are rendered useless because their genetic material is simply incompatible. Even though two species may be physically able to have sex, the real crucial step in sexual reproduction, the combining of egg and sperm and their genetic payloads, cannot take place for any number of physiological reasons (e.g., different numbers of chromosomes). But there are plenty of cases, particularly among birds, where two species mate, their genetic material combines, and they do produce offspring. In those cases another type of barrier might come into play. The hybrid offspring might itself be rendered infertile by complications caused by having a genome made up of heterospecific DNA, and is itself incapable of reproducing. The freak show ends there. These kinds of barriers, prezygotal (the ones that stop species from mating in the first place) and postzygotal (the ones that stop hybrids themselves from passing on their own mixed genes), tend to be strong between species that have experienced long periods of evolutionary divergence. But in species with less evolutionary history separating them, hybridization does occur, and at least among some species, with astonishing frequency.

Hybrids are a problematic lot. They are problematic for biologists who want a neat and tidy way of defining species. For the past two centuries, naturalists and biologists have argued over exactly what a species is. It’s not an unimportant, arcane thing; the concept of a species is fundamental to our understanding of biology. We use the word to describe diversity, to distinguish one type of organism from another. Birders keep lists of species. We have legislation to protect rare and disappearing species. But what exactly is a species? There are a myriad of definitions. The most widely used has been and continues to be the biological species concept. By this definition, a species is defined as any group of organisms that can produce fertile offspring. It’s a difficult definition to apply widely in biology without running into problems, not the least of which is how do you treat species that hybridize? The biological species concept would suggest that any organisms which can hybridize and produce fertile offspring (offspring that can themselves go on to produce young of their own) are the same species. Period. No ifs, ands or buts. If you stuck firmly to this definition, you’d have to concede that no matter how different two organisms look, sound, smell or taste, no matter how ecologically dissimilar they were, if they could produce fertile kids, they’d be the same species. That’s not exactly a satisfactory definition, I think you’ll agree. Biology is never that simple. For example, what if the frequency of hybridization is rare? What if species never interact in nature because of geographic barriers, but in captive situations they readily interbreed? But I digress. I don't want to get into an endless discussion of species concepts here. Let's talk more about hybridization itself.

A strange bird was netted in Wethersfield, New York in June 2006. The ornithologist who pulled it from the mist net must have said something like "what the fuck is this?!" It may not be a direct quote, but I’m sure it was an approximation of their thoughts. The bird was unlike anything in any bird book, anywhere. It was warbler (family Parulidae) to be sure, and it would eventually be given the name Junkin’s Warbler. The bird was photographed and released, as per the researchers’ protocol. It was clearly a hybrid, but of what two species? The photos and descriptions of the bird were shown around. Everyone who saw it took their best guess. But best guesses just don’t cut it among bird people. The bird had to be identified! So an effort was made to track it down and catch it again.

Success! The mystery warbler was recaptured, looked at by a few more ornithologists, and had a few feathers plucked. DNA was obtained and sequenced from those feathers. The lab at Cornell University already had a genetic sequence database of almost all the warbler species and it was just a matter of comparing the genetic sequence of the Junkin’s Warbler to the others in the database. Mitochondrial DNA (the mtDNA), which is only maternially inherited was used to determine that the mother was a Kentucky Warbler (Geothlypis formosa). Nuclear DNA comes from both parents, one copy is passed on by the mother, the other is passed on by the father. One nuclear DNA sequence obviously matched Kentucky Warbler; that came from the mother. The other sequence matched Mourning Warbler (Geothlypis philadelphia).

The breeding ranges of Kentucky and Mourning Warblers overlap only slightly in Pennsylvania so their chance to hybridize under normal circumstances is rather limited. But if one of those species somehow got itself settled out of its usual range during the breeding season, it may have had no choice but to mate with a member of another species or mate not all. As we all know, the drive for sex is a strong one, and sometimes you just have to make due. Male warblers often return very near their place of hatching, while females often disperse more widely. The Junkin’s Warbler was thought to be a male, but apparently that was never fully confirmed. That could mean that its place of capture, in western New York, was close to its place of birth, and this location is one at which Kentucky Warbler would normally not breed, but where Mourning Warblers normally do. If a female Kentucky Warbler decided to settle in western New York, for some reason, where she had no chance of finding a conspecific male, she’d have no choice but to mate with a male from another species.

The Junkin's Warbler is just one of many examples of hybridization among warblers (family Parulidae). The warblers are a favourite group of mine: they're pretty, they're vocal, they're widespread and ubiquitous. But for me, the real fascination with warblers stems from their natural history, which by virtue of their diversity and their wide geographic distribution, covering a huge swath of the Americas from the Alaskan tree line to the Argentine Paraná wetlands, warblers have evolved a wide array of strategies for tackling all of life's challenges. A kind of beautiful intrigue also lies in their evolutionary history, one in which climate and biogeography, as well as natural and sexual selection, have conspired to shape each species into the forms we recognize today. When it comes to hybridization, they are no less intriguing. This is the first essay in a three part series on hybridization in warblers called Infus'd Betwixt.

Decades ago Kenneth Parkes, for whom the waterthrush genus Parkesia is named, thought he saw some patterns in the way warblers hybridize. Hybrids, he said, could essentially be grouped in two types: those formed between closely related species and those formed between more distantly related species. When all known hybrid types were considered, it was apparent that there were more examples of occasional hybrid pairings between distantly related species than between closely related species. Certainly, some hybrids were the result of two very closely related species pairing, but such cases were more uncommon except among a few select groups of sister species. Sister species are those that share a very recent common ancestor. Examples include Golden-winged (Vermivora chrysoptera) and Blue-winged Warblers (Vermivora cyanoptera), Northern (Setophaga americana) and Tropical Parulas (Setophaga pitiayumi), and Golden-fronted (Myioborus ornatus) and Spectacled Whitestarts (Myioborus melanocephalus).

In Parkes’ reckoning, most of the hybrid pairings were between members of different genera. The going theory of the day was that isolating signals – things like song or plumage characteristics – worked most strongly among closely related species (the exception was among a few sister species that hybridized with some regularity probably because they were still just a little too similar), but had become relaxed between more distantly related species. This pattern of hybridization came to be known as Parkes’ Paradox.

It was a paradox because normally we think of closely related species as being the most similar and therefore more likely to hybridize than distantly related, more differentiated species. Distantly related species are more different from one another, generally speaking, because the long periods they’ve had to evolve differences. True, two closely related species can look and sound as different from each other as two distantly related species. But one thing that closely related species usually do share, that distantly related species usually do not are their ecologies. Species that occupy the same habitats, place their nests in the same locations or forage for the same foods, should in theory, be more suitable candidates for successful hybridization than species that differ in all these traits. That makes sense, no? For Kenneth Parkes and others interested in warbler hybridization the pattern was clear. But did it have any evolutionary resonance? Was Parkes’ Paradox telling us something important about speciation and species recognition?

Thirty four years after Parkes’ paper another look at patterns of hybridization in warblers reveals something entirely different. I did a quick search of the literature and came up with 39 hybrid combinations, though there are probably more. Of these, 27 of the hybrid combinations were between members of the same genus (intrageneric) and only 12 were between members of different genera (intergeneric). The makes 69% intrageneric and 31% intergeneric. Why the disparity between Parkes’ Paradox and the numbers I’ve just presented? The reason is twofold. First, since Parkes’ time many new hybrid combinations have been discovered. Second, the classification of warblers today is markedly different from that Parkes knew in 1978. The most recent phylogenetic hypothesis for the Parulidae represents a vast rearrangement of species within and between genera compared to the classification Parkes was working with in the 1970's. In effect, many of Parkes’ intergeneric hybrids were actually intrageneric. Without the benefit of modern genetics to peer inside the genomes of all the warblers Parkes had no way to know this. Interestingly, all of Parkes’ intergeneric hybrid pairs are still classified as such. A number of the intergeneric hybrid pairings that Parkes cited are now considered to be intragenetic pairs. For example, Northern parula (formerly Parula americana) is now classificed in the genus Setophaga, thus making a formerly intrageneric hybrid pairing with American Redstart (Setophaga ruticilla) an intrageneric union. But for the most part, the intrageneric pairings outnumber the intergeneric pairings in the sheer number of different combinations reported in the literature. So Parkes' Paradox has been rendered a little less paradoxical.

Some warbler hybrids occur frequently enough, to have common names of their own: Brewster’s and Lawrence’s (Golden-winged × Blue-winged Warbler and various backcross combinations), Sutton’s (Yellow-throated Warbler [Setophaga dominica] × Northern Parula) and Cincinnati (Blue-winged × Kentucky Warbler). Early ornithologists seemed unwilling or unable to accept the occurrence of hybrids; Brewster’s, Lawrence’s and Cincinnati warblers were all considered new species when they were first collected in the 1870’s. They were all anointed with the unwieldy genus name Helminthophaga and the species leucobronchialis, lawrencii and cincinnatiensis, respectively. It wasn't until a decade or two later that they were finally recognized as hybrids.

It’s not as though the concept of hybridization was a new one in biology. Darwin himself thought long and hard about it. He wrote about it too. While composing his thoughts for the Origin of Species he wrestled with hybridization, trying to decide if it was possibly an important source of variation and whether it could lead to the advent of new species. Later, in Variation of Animals and Plants under Domestication, he addressed hybridization again, asserting that it could in fact be a cause of speciation. Among ornithologists working during the late 1800’s and early 1900’s, hybridization was not yet well understood. There was no helpful genetic testing at the time, just plumage, song and behavioural clues to go on. In addition to being called new species, hybrids were called "spontaneous mutants" and colour morphs of already known species. It wasn’t until 1908 that Mendelian genetics were used to illustrate how Golden-winged × Blue-winged Warbler hybrids inherited traits from their respective parents that ornithologists began to readily accept the reality of hybridization among the warblers.

Among the "named" hybrids, Cincinnati Warbler is one of the rarest. It doesn’t occur as frequently in nature as the Brewster’s or even Lawrence’s Warblers. When it was first collected in 1880 it was one of a kind. But in 1948 another suspicious-looking warbler appeared; it was thought to be a Blue-winged × Mourning Warbler hybrid. The specimens were compared to each other, to their putative parent species and to all other warblers. Based on the exhaustive comparison it looked as though both birds were indeed of Blue-winged Warbler parentage on one side. However, the original specimen from 1880 bird from Ohio appeared to be a backcross between a pure Blue-winged and a hybrid Blue-winged × Kentucky Warbler. The 1948 bird from Michigan was considered to be the product of a pure Blue-winged and pure Kentucky.

Backcrossing makes the already challenging problem of diagnosing a hybrid bird’s parentage more difficult. To understand the concept of backcrossing you need to think about generations. When a Blue-winged Warbler and a Kentucky Warbler mate and produce a Cincinnati Warbler the Cincinnati Warbler gets labeled as F1 – filial generation one. Provided this hybrid is fertile, and F1's often are among warblers, they can go on to mate and produce offspring with one of their parent species – that’s a backcross. The resultant offspring of a backcross would be called F2. If hybrids were frequent enough in a population, and they sometimes are among certain warblers, two F1's may find each other and mate. They will produce what are called double-cross hybrids (they are also F2's). Backcrossing can create a plethora of confusing-looking and -sounding hybrids. Perhaps the most important example of backcrossing mania can be found among the Vermivora.

To fully understand the Golden-winged × Blue-winged Warbler backcross phenomenon, its worth looking at the concept of allopatric speciation. No, I'm not kidding, its actually a rather important piece step in the history of these hybrids. One of the primary ways new bird species arise is through the isolation of an ancestral species in two or more pockets of habitat. When no gene flow occurs between those insular populations, the birds differentiate from one another and eventually become new species. This is the process of allopatric speciation. Over time, species which arose in allopatry come into contact with each other. This happens naturally all the time: mountain ranges erode, ocean basins close, forests colonize grasslands and species meet each other as a result. If contact happens before those species are fully formed, hybridization can occur. It can occur so extensively that where there were once two species, given enough time, they can become one. When two species rejoin in this way naturally, and it has probably happened countless times over the millennia, it’s a natural curiosity. It’s a real world demonstration of evolutionary principles, the kind of thing that keeps biologists awake at night giddy with excitement. But when it is caused by humans, and it definitely has been in latter centuries, it’s an entirely separate thing. It’s the sort of thing that keeps biologists awake at night for another reason all together. I'll address that issue further in Part 2 of Infus'd Betwixt.

Two Days with Bruce

Massasauga Rattlesnake (Sistrurus catenatus).

Photo: Mark Conboy

A wrong turn on an unfamiliar trail can lead to confusion, frustration and the unenviable job of backtracking across some slippery talus slope or through a knee-deep swamp. On the other hand, it can also lead to a wonderful discovery. By way of example, I took a wrong turn off a Bruce Peninsula trail earlier this month, and I was rewarded for my buffoonery by an encounter with one of Ontario's least often seen and most misunderstood reptiles: the Massasauga Rattlesnake (Sistrurus catenatus). I went to the Bruce Peninsula specifically in search of rattlesnakes and much to my delight what I found was a land full of additional surprises.

The focus of my explorations was Lion's Head Provincial Nature Reserve, the real treasure of the Bruce Peninsula, with one of most dramatic coastlines on the Great Lakes: shinning white cliffs that support ancient forests of stunted Eastern White Cedars (Thuja occidentalis). The cliffs plunge into a band of forest which in turn sweeps down to the crystalline waters Georgian Bay. Upon the cliff tops themselves, the forest, dense with Eastern White Cedar and Balsam Fir (Abies balsamea), hides a geological wonderland of glacial potholes, acid-worn caves, bottomless crags, overhanging rock faces, and erosion-sculpted boulders of ten thousand different forms.

I started on the trail at six o-clock one evening, into a forest alive with the ethereal whistling of Swainson's Thrushes (Catharus ustulatus), which lent the evening air a subdued and angelic texture. I worked my way east along the ridge top from one spectacular lookout to another. To the north I could see the peninsula stretching far off, a vast swath of seemingly undisturbed forest and coastline. Not a breath of sound, not a light, not a tower, not a road, not a cabin betrayed the illusion of vast and insurmountable wilderness. I knew what truly lay out there, hidden by distance, green forest, and heaving geology. Of course I knew of the towns and cottages, the lighthouses, the roads and their stinking cars. But I let my mind imagine a world unsullied by humans, a wild land stretching from Lion's Head to the tip of the peninsula and beyond to Manitoulan Island, to the North Shore, across the boreal hinterlands, to the freezing waters of Hudson Bay. A world teeming with game and fish and winding trails. The cries of a raven brought me back to reality. And so I lifted my pack, and hit the trail once again.

The cliffs upon which I walked dropped down for ninety or one hundred metres into the forest below. Far from smooth, the cliffs were undercut, overhanging ominously, inviting me to stand upon many a narrow slab, as though to dare fate. The cliff faces were pocked by small depressions and shelves, and it was upon those little natural balconies their existed a most remarkable community of ancient trees, a vertical forest of centuries-old Eastern White Cedars. Many of the cedars, though small and spindly, more like shrubs than proper trees, were two, three, four or even eight centuries old. The oldest yet discovered at Lion's Head is over 1,300 years old and for all its age is only about seven metres tall.

Dolostone cliffs at Lion's Head Provincial Nature Reserve with Eastern White Cedars (Thuja occidentalis).

Photo: Mark Conboy

The cliff-side cedars are natural bonsais, sculpted by centuries of extraordinarily slow growth on water- and nutrient-poor dolostone, twisted by driving winds, polished by blowing snow, and cracked by frost. Their trunks and limbs are gnarled, knotted and ropy. They do look truly ancient, truly sage-like. Many of the cedars appear to be half dead, and indeed they are. Eastern White Cedars, perhaps unique among Ontario trees, grow in sections; one portion of the root mass feeds one portion of the crown. In this way the left side of a cedar may die as the roots which feed it run low on nutrients while the right side of the tree continues to thrive, its roots having managed to find sufficient resources. This segmenting, may be one of the reasons why cedars have such staying power, where other less versatile species simply can't survive. Over the past 10,000 years, fire has periodically burned along the cliff tops, but the cliff faces appear to have been spared, and so the trees were allowed to grow old, excessively old. Even that zealous craze for wood and civilization, the rampant forest clearing, left the difficult-to-access vertical forests unmolested. The longevity of the ancient cedar forests it would seem, is a lucky coincidence of topography: safe there on the cliff sides from the ravages of fire and man. But not entirely safe.

Perhaps the single biggest threat that the ancient cedars face todays is rock climbers. The cliffs of Lion's Head are a popular sport climbing destination. It's easy to spot the most well-climbed routes: lichens have been rubbed away, duff has been swept from the tiny ledges, and in some rare cases, cedar branches have been cut. It seems that most of the pruning, and it hasn't been excessive, was done before the agelessness of the cedars was discovered. Though, if a saw-wielding climber had bothered to look at the annual growth rings of the limbs they were pruning it may have been obvious just how old those trees were. Today, the climbing community has more awareness of the ancient trees, and thankfully, disturbance is less of an issue as it was in the past. To share the cliff faces with age-old trees, that can only add to the exhilaration of the climb, can it not?

Cryptoendolithic organisms (not from the Bruce Peninsula in this example) growing inside a rock.

Photo: Guillaume Dargaud (Wikimedia Commons)

Eastern White Cedar belongs to the family Arborvitae, from the Latin, tree (arbor) of life (vitae). Indeed a fitting appellation for this long-lived species. The cedars though are not the only ancient cliff dwellers. The roughly textured dolostone supports an array of lichens, tiny symbiotic organisms that give colour to the cliff faces. Hidden within the pores of the rocks themselves is even more unlikely and more bizarre life, cryptoendolithic organisms. Nine species of cyanobacteria and 13 species of green algae living 1-5 mm deep within the porous rock have been recorded on the Bruce Peninsula. From the right vantage point these colonies of microorganisms can be seen as black stains on the white dolostone. The cyanobacteria and algae aren't just innocuous cliff dwellers, but instead play a role in the nutrient cycling of the cliff ecosystem, absorbing sunlight through the semi-translucent rock, and imputing nutrients into an otherwise depauperate ecosystem. The Bruce Peninsula is one of only a handful of places on Earth where cryptoendolithic organisms have been studied.
After several kilometres of fairly rugged trail I began a descent towards the coastline past thick slabs of dolostone that fell from the cliffs centuries ago, each now supporting their own garden of trees and shrubs. The Swainson's Thrushes sang all around as I dropped further and further down. Just before reaching the cobble beach, the trail passed below a massive overhanging slab. The slab protruded from the forest like a great bird's beak. Eight metres long and almost as wide, it sheltered a patch of bare soil, starved of rain water and sunshine, nothing grew there, a stark contrast to the thick forests that surrounded the outcrop. It's a fantastic natural sculpture, unexpected along this trail, while simultaneously not out of place in this land of geological wonder.

Earlier on the trail I came across several potholes, including one with the whimsical name, the Giant's Cauldron. These potholes or kettles were formed beneath glacial ice, where free flowing water formed a small whorlpool. Stones gathered up by the whirlpool were spun around and around wearing holes into the rock. The potholes stopped growing when the water flow subsided or the stones that chiselled them eroded to nothing. The Giant's Cauldron was about the size of, well, a very large cauldron, but just down the trail was an even more impressive one, the Lion's Head Pothole. This one was at least three metres deep and about a metre and half in diameter. There was a wonderful little portal in its side, that allowed one to squeeze right inside of the pothole. From within, the smooth stone wall directed your out of a sky light towards a canopy of Sugar Maple (Acer saccharum) and American Beech (Fagus grandifolia). Standing literally within the rock, an eerie silence prevailed.

The Lion's Head Potholes claims another curious naturalist.

Photo: Mark Conboy

The trail stepped over dozens of grykes, joints in the rock widened by weathering of the basic dolostone by slightly acidic rainwater. Small caves peaked out of the leaf litter; I wondered if they led to larger caves, caverns, perhaps as yet unexplored. The trail was rocky and never flat, each step either up or down over pock-marked rock. The pocks, or vugs in geological parlance, were formed as the dolostone itself was formed. Dolostone is essentially limestone that has been infused with magnesium. The original limestone, the precursor to the dolostone I navigated over all evening, was laid down in a massive coral reef sometime during the Silurian period (443 to 416 million years ago). This reef, which essentially forms the backbone of the Niagara Escarpment (of which the Bruce Peninsula is the northernmost extension), was formed by the growth and death of countless generations of corals and other sea creatures whose calcium carbonate shells became consolidated into solid limestone over eons. That limestone was eventually pushed underground where it was infused with highly saline magnesium-rich groundwater. The magnesium replaced the lime, changing the limestone to dolostone. That conversion resulted in some loss of rock volume, and that's how the vugs were formed. Had this dolomitization process not occurred we might not have the dramatic scenery of the Bruce Peninsula we see today. Dolostone, though it can be weathered, as evidenced by the potholes, grykes and caves along the trail, and large piles of talus below the cliffs, is far less resistant to erosion than limestone. Perhaps the limestone would have been eroded millennia ago, leaving a more or less flat shoreline, similar to the Peninsula's western shore. But the dolostone has persisted, giving us the dramatic views and ancient cedar forests of the Lion's Head.

The trail lead to a pleasant campsite under the shade of cedars and Red Maples (Acer rubrum). I pitched my tent near the cobble beach and settled in for a night apart from the rest of humankind.

In the morning, I found myself ascending to the cliff tops once again. Black-throated Green Warblers (Setophaga virens) were singing in profusion; it seemed that I was never out of earshot of one all morning. The woods were simply overrun with those pretty little songsters, but it wasn't long before my attention turned from the birds to the trailside plants. The Bruce Peninsula supports over forty species of orchids, most of which I didn't expect to find the Lion's Head; they are inhabitants of bogs, fens, swamps and alavars - habitats I simply didn't pass through on my hike. But these high and dry cedar woods do support a handful of species, including two biogeographical oddities: Menzies' Rattlesnake Plantain (Goodyera oblongifolia) and Alaska Orchid (Piperia unalascensis).

The tiny flowers of an Alaska Orchid (Piperia unalascensis), a western species with a disjunct Great Lake population.

Photo: Mark Conboy

Both the rattlesnake plantain and the Alaska Orchid are western disjunct species. Both are primarily distributed in western North America, but they can also be found in pockets isolated pockets elsewhere. The Alaska Orchid is the more extreme example of this pattern. Its main distribution extends from southern Alaska to Baja California. Disjunct populations occur on the Great Plains, in eastern Canada and of course, in the Great Lakes Basin. It's likely that Alaska Orchid enjoyed a much broader prehistoric distribution, that linked all of the disjunct populations to the species' main western range. For some reason, the Alaska Orchid's range contracted into the discrete populations we see today. Though less dramatically, the rattlesnake plantain also has a similar  disjunct pattern and probably has a similar biogeographic history. Perhaps it was the presence of such disjunct species that caused American botanist M.L. Fernald in the 1920's, to hypothesize that the Bruce Peninsula was an unglaciated relict, harbouring species that once enjoyed a wide preglacial distribution in an ice-free refugium. We now know that unequivically, the Peninsula was completely ice-covered for several thousand years and that the disjunct distribution of orchids and other species must be explained by other means.

Another plant caught my attention on several occasions throughout the hike. The Northern Holly Fern (Polystichum lonchitis) is a relatively rare species in Ontario, but evidently there is a healthy population on the Bruce Peninsula. Beyond ancient trees, disjunct orchids, and unusual ferns, the Bruce Peninsula harbours other botanical treasures, including significant concentrations of range-restricted Dwarf Lake Iris (Iris lacustris), Lakeside Daisy (Hymenoxys herbacea), and Tuberous Indian-plantain (Arnoglossum plantagineum).

Northern Holly Fern (Polystichum lonchitis) and Maidenhair Spleenwort (Asplenium trichomanes).

Photo: Mark Conboy

But as I said, the Massasauga Rattlesnake was the main reason I visited the Bruce Peninsula. Rattlesnakes were extirpated from my home county of Norfolk and most of the rest of Southwestern Ontario long ago, although there are remnant isolated populations at either end of Lake Erie. The species' last true haven is the Bruce Peninsula and the Georgian Bay coast. In the case of Ontario's Massasauga Rattlesnakes, there is a significant amount of genetic differentiation and geographical isolation between the Bruce Peninsula and Georgian Bay populations. Even though these two rattlesnake populations exist in close proximity, they are actually rather isolated from one another, and that can have some important biological consequences. 

Gene flow is important to maintaining genetic diversity, and good genetic diversity can help with disease resistance and adaptation to changing environmental conditions. Isolated populations of snakes and other organisms tend to have limited genetic diversity because of a lack of immigration from other populations (immigrants bring new genetic materials) and inbreeding.

Massasauga Rattlesnake (Sistrurus catenatus).

Photo: Mark Conboy

The snakes of the Bruce Peninsula are isolated from those of eastern Georgian Bay by water (and also intensive agriculture and road development on the southern part of the peninsula). Massasaugas, despite their fondness for wetlands, are unable or unwilling to undertake long distance swims, so the Bruce Peninsula snakes are effectively stuck on their own island, separate from their conspecifics to the east. Indeed open water is such an effective barrier to rattlesnake dispersal that Lyal Island, a mere 1.3 km off the western shore of the Bruce Peninsula, harbours its own genetically distinct population of Massasaugas. At some time in the past, Masassaugas colonized the island, but since that time, emigration from the main peninsula population has been all but nonexistent, allowing the Lyal Island snakes to develop their own genetic identities, apart from the Bruce Peninsula snakes.

 

Isolated populations are not necessarily a bad thing, especially if they are large, and genetic diversity can be maintained to some degree through mutations; so the Bruce Peninsula rattlesnakes are not likely to disappear because of inbreeding or something like that, at least not any time soon. What is most interesting about the isolation and genetic uniqueness of the peninsula's rattlesnakes (and it's orchids too, no doubt), is that it demonstrates a simple biological fact: not all members of one species are the same. I argue that each and every distinctive population should be conserved as though it were a distinctive species. In the case of Massasauga Rattlesnakes, we need to insure that the Bruce Peninsula population is receives proper conservation, and so too does the Lyal Island population and the many genetically discrete populations on Georgian Bay's east coast, each as though they were a different species. It would certainly be a tall order, but it would be the right conservation approach.

Bioluminescent Biters

Smooth Lanternshark (Etmopterus pusillus)

Photo: Brandi Noble (Wikimedia Commons)

Bioluminescence, the production of light by organisms, is a marvelous ability possessed by a broad range of species including troglodytic glow worms, forest fireflies, thumb-sized click beetles, Caribbean zooplankton, parasitic fungi and even lowly bacteria. There are hundreds of bioluminescent species on land and in water, but arguably, the phenomenon finds its finest (and trippiest) expression in the murky ocean depths.

Deep sea organisms live in a dark world, with little or no sunlight penetration. But its not a world entirely without light, thanks to bioluminescence. Most deep sea organisms utilize bioluminescence for communication, warning, or hunting, by combining a light-emitting luciferin pigment (the most common of which is coelentarazine) with an oxidative luciferase enzyme; the result, as luciferin reacts with oxygen, is the production of light.

Perhaps the most famous of these deep sea illuminators are the anglerfishes, diverse array of whimsically named species from a suite of different families, including goosefishes, frogfishes, handfishes, sea toads, footballfishes, dreamers, whipnoses and seadevils. Typical anglerfish, let's take the Humpback Anglerfish (Melanocetus johnsonii), which is perhaps better known as the Black Seadevil, thanks to its meteoric rise to fame on YouTube in 2014, features a light-producing organ called a esca, which is mounted on a specialized ray called an illicium. The esca hangs in front of the anglerfish's generously-toothed and highly destendable mouth, and illuminates with the help of bioluminescent symbiotic bacteria. The light serves to attract potential prey and mates.

Beyond anglerfish, there is a ensemble of other bioluminescent deep sea denizens, including squid, snails, worms, jellies, an astounding diversity of zooplankton, and many more fish. Among the more unique are the loosejaws (Malacosteus spp.), which produce a red bioluminescence. Red light cannot be seen by most of the loosejaw's prey and so this flashlight-wielding predator has a distinct hunting advantage - it can see its prey, but its prey can't see it. Most bioluminescent deep sea organisms haven't received much scientific study, but one group that has are the lanternsharks (Etmopterus spp.), and they've proven even more interesting than your average bathypelagic swimmer.

Lanternsharks (family Etmopteridae), are a diverse lineage found all over the world's oceans, most of them living between 200 and 5000 m deep. As their name suggests, lanternsharks are bioluminescent, but they aren't the only sharks that sparkle and shine: cookiecutter sharks (Isistius spp.), Viper Dogfish (Trigonognathus kabeyi), Pygmy Shark (Euprotomicrus bisinatus), and Taillight Shark (Euprotomicroides zantedeschia), for example, do so too. But it is among the 40 species (others probably await discovery) of lanternsharks that bioluminescence is most pronounced. In fact, their bioluminescence may have played an important role in promoting the great diversity of Etmopterus we see in the world's oceans today.

Most of the lanternsharks have bioluminescent organs (photophores) on their bellies and their sides, although some species don't seem to have any at all. Sadly, the only lanternshark that occurs in Canadian waters, Great Lanternshark (Etmopterus princeps), doesn't glow, though, strangely, it lives deeper than many of the other etmopterids, down to 4500 m, where having some bioluminescent abilities ought to be highly advantageous. But for those species that do light up the abyssal depths, they do so in a three of different ways. Their bellies are covered in photophores that glow a dull blue and are used as a form of camouflage called counter-illumination. Most lanternsharks are less than a metre long, thus potential prey for many larger fish. Even in the near-complete darkness of the deep sea, the large sensitive eyes of many predatory fish can detect the silhouettes of their prey swimming above them, but the subtly glowing bellies of lanternsharks makes their silhouettes invisible against the faint background of blue light emanating from above. Lanternsharks, in effect, hide in plain sight. Many surface dwelling fish have a similar but less sophisticated adaptation called counter-shading, wherein their bellies are a light shade to match the sky above, thus making them more difficult for predators to spot from below.

Other sets of  photophores lines the flanks of lanternsharks  and some species have them on their backs as well. These photophores, rather than acting as camouflage, make their bearers more obvious, either as aposmatic (warning) signals to potential predators or as advertisements to potential mates. We're all familiar with aposmatic colours, bees and wasps for example, are patterned black and yellow to announce to predators that they shouldn't be messed with, lest they deliver a painful sting. In a similar fashion, lantersharks have generously large spines at the base of both dorsal fins, and at least one species, the Velvet Belly (Etmopterus spinax), illuminates its spines to advertise this formidable defense mechanism. The researchers who made this discovery facetiously called the illuminated spines lightsabers.

Green Lanternshark (Etmopterus virens). The dark patch on the belly is a concentration of bioluminescent photophores used in counter-illumination, while the linear dark patches near the base of the tail are photophores used in species recognition. Each dorsal fin sports a spine at its lead edge. 

Photo: Brandi Noble (Wikimedia Commons)

Lanternsharks also employ bioluminescence when advertising to potential mates. The band of photophores along the flanks and tail base are unique for each species. This novel adaptation may have allowed Etmopterus to rapidly diversify into more species than almost any other shark genus. Species-specific photophore patterns act as a means of genetic isolation, keeping species from hybridizing. Just as bird species tell each other apart by the differences they display in plumage, lanternsharks distinguish between members of their species (potential mates) and other species (non-suitable mates) by the unique light patterns each produces. A lanternshark's light display isn't terribly bright, it doesn't shine like a spotlight through the pelagic depths, instead it's more subdued, often visible from only a few metres away. But it's enough to do the trick, especially when aided by special ocular adaptations that make lanternshark eyes extremely sensitive. What to a human observer may seem like a meagre glow emanating from the flank of a Splendid Lanternshark (Etmopterus splendidus), may actually appear to be a magnificent lightshow to the sharks themselves.