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Picidae (2 Viewers)

Jente Ottenburghs and Michaël P. J. Nicolaï (2024) Hybridization constrains the evolution of mimicry complexes in woodpeckers. Journal of Avian Biology, published online 26 February 2024.
https://doi.org/10.1111/jav.03228

Abstract
The evolution of interspecific mimicry does not always result in perfect resemblance between mimics and models. Differences between members of a mimicry complex can be explained by genetic or developmental constraints. Alternatively, imperfect mimicry might be the outcome of a tradeoff between multiple selective pressures. In this study, we explored the evolutionary conflict between mimicry and hybridization in woodpeckers. Based on the selective tradeoff hypothesis, we expected that mimicry complexes will start to evolve once the constraint of maladaptive hybridization is relaxed. Hence, we predicted limited overlap in the divergence times between hybridizing species pairs and members of a mimicry complex. This prediction was supported by clear tipping point in the probability of hybridization and mimicry at ca 9 million years of divergence. Around this timepoint, the probability of hybridization approaches zero while the probability of belonging to a mimicry complex increases. This finding is only correlational and remains to be confirmed in other taxonomic groups. Nonetheless, our results suggest a selective tradeoff between evolving interspecific mimicry and avoiding maladaptive hybridization in woodpeckers.

I'm always shocked at the strength of faith in this idea of woodpecker "mimicry," especially in the absence of behavioral studies which establish such a thing. This paper flatly states mimicry "evolved several times" in woodpeckers based on Miller (who said that geographic overlap of similar plumage is "suggesting occasional strong selection for interspecific mimicry") Shemya (who investigated how rapid diversification rate, hybridization, convergence and potential mimicry complicate woodpecker phylogeny) and Benz, who simply suggested based on Celeus/Drycopus phylogeny that mimicry be explored in the Brazilian Atlantic Forest community.

Mimicry is just one of several reasons that birds with a common ancestry in the same habitat and similar niche might look like one another. I'm still waiting for any solid behavioral study to indicate that it even occurs, let alone is such a powerful driving force in woodpecker genetics all over the world. I don't know why "mimicry" has been so readily accepted as an explanation for Picidae alone - where are the "mimicry" papers for the tyrant flycatchers, the tinamous, treecreepers, the Larus gulls and on and on?
 
I'm always shocked at the strength of faith in this idea of woodpecker "mimicry," especially in the absence of behavioral studies which establish such a thing. This paper flatly states mimicry "evolved several times" in woodpeckers based on Miller (who said that geographic overlap of similar plumage is "suggesting occasional strong selection for interspecific mimicry") Shemya (who investigated how rapid diversification rate, hybridization, convergence and potential mimicry complicate woodpecker phylogeny) and Benz, who simply suggested based on Celeus/Drycopus phylogeny that mimicry be explored in the Brazilian Atlantic Forest community.

Mimicry is just one of several reasons that birds with a common ancestry in the same habitat and similar niche might look like one another. I'm still waiting for any solid behavioral study to indicate that it even occurs, let alone is such a powerful driving force in woodpecker genetics all over the world. I don't know why "mimicry" has been so readily accepted as an explanation for Picidae alone - where are the "mimicry" papers for the tyrant flycatchers, the tinamous, treecreepers, the Larus gulls and on and on?
Interesting! But isn't the point that they don't have a common ancestry? Yes, they're all woodpeckers, but Lesser Spotted is only a distant relative to White-backed, Middle Spotted to Great Spotted, Downy to Hairy and so on.
 
I think the the fact that the flamebacks on Sri Lanka (Chrysocolaptes stricklandi (Crimson-backed Flameback) and Dinopium psarodes (Red-backed Flameback)) are red-backed, while their closest relatives in mainland Asia are yellow-backed can also most easily be explained by mimicry.
Tinamous and woodcreepers are just cryptically coloured. However, the "kiskadees" could be an interesting case study.
 
Without wading into the broader discussion of how much it's mimicry and how much it's highly conservative phenotypical expression, I think the aforementioned case of Dryocopus galeatus actually being a Celeus but being the only member of the genus Celeus to resemble a Dryocopus is actually difficult to explain without considering mimicry...
 
I was confused by the abstract, because mimicry in a lot of animals is related to looking like something that is dangerous when you yourself are not dangerous. What benefit would a woodpecker get from mimicking another woodpecker?
 
“But within birds, a largely overlooked type of mimicry instead serves to reduce aggressive attack from competitors. Subtle differences in weight and size can confer a huge advantage in a competitive skirmish, just like in a boxing match. By deceptively mimicking the appearance of a larger, socially dominant species, the smaller bird is able to avoid attack.”

Similarly, orioles mimic friarbirds in eastern Wallacea.
 
Interesting! But isn't the point that they don't have a common ancestry? Yes, they're all woodpeckers, but Lesser Spotted is only a distant relative to White-backed, Middle Spotted to Great Spotted, Downy to Hairy and so on.
Do we know that they don't all share a pied ancestor? In Biology 101 we talk about how shared characteristics are often more parsimonious to be basal to a phylogeny, rather than derived over and over again. Whether that phylogeny is Dendrocoptes or Picidae shouldn't really matter.
 
I think the the fact that the flamebacks on Sri Lanka (Chrysocolaptes stricklandi (Crimson-backed Flameback) and Dinopium psarodes (Red-backed Flameback)) are red-backed, while their closest relatives in mainland Asia are yellow-backed can also most easily be explained by mimicry.
Tinamous and woodcreepers are just cryptically coloured. However, the "kiskadees" could be an interesting case study.
To take the flameback example - what is the evidence that there isn't something about Sri Lanka that selects towards red instead of yellow? A predator's vision... forest structure... dietary differences or anything else affecting carotenoids... an endemic parasite or disease... something affecting time budget during low light hours.... All of these and more need to be ruled out before we can say something is most easily explained by mimicry. Unless, of course, there is a behavioral study that reveals the mimicry mechanism - but I'm not aware of one.

I just feel like if there were SO MUCH woodpecker mimicry in so many taxa everywhere from Europe to Sri Lanka to Brazil to Ohio, wouldn't a mechanism be so very obvious? Wouldn't they be antagonizing each other so much that its clear why this selective pressure is so intense? Moreso than, for example, Yellowlegs or Accipiters, to add other interesting case studies?
 
Without wading into the broader discussion of how much it's mimicry and how much it's highly conservative phenotypical expression, I think the aforementioned case of Dryocopus galeatus actually being a Celeus but being the only member of the genus Celeus to resemble a Dryocopus is actually difficult to explain without considering mimicry...
I agree that it is difficult to explain without convergence... but why mimicry instead of any other kind?
 
See also Leighton et al. (2018) on the possibility that downy woodpeckers mimic hairies.
However, note from the abstract "Our empirical data thus offers no support for the strict Interspecific social dominance mimicry (ISDM) hypothesis as an explanation for downy–hairy woodpecker plumage convergence."

Leighton speculates that there may be mimicry in response to some third-party species... but what species would that be? What benefit does that confer on one or both species?

I don't dispute that there is some sort of convergence going on - but not all convergence is mimicry.
 
I agree that it is difficult to explain without convergence... but why mimicry instead of any other kind?

I am no expert here so my opinion is worth less than the paper it's not even printed on. Shy of a better hypothesis, I'm simply applying Occam's Razor to what I believe I know of the situation with Woodpeckers and with mimicry in general. I would be surprised if the situation isn't more complex across all of Picidae, and if there aren't multiple mechanisms at work and if the cases don't differ from each other. But I'd also be surprised if mimicry weren't a factor with Celeus galeatus.

Overall though I agree with your point - we know very little, really. When you start looking much more broadly, the cases that are hard to even try to offer a simple explanation to far outweigh the cases where one can say "hey it seemingly makes sense that this could be mimicry for reason X."

Juvenile Cinereous Mourners looking like toxic caterpillars is mind-bogglingy cool and seemingly easy to say "well the obvious explanation makes a lot of sense so barring information to the contrary let's work with that as our current axiom."

Non-toxic insects and non-venomous snakes looking like their toxic / venomous brethren also seems easy to explain and barring a better hypothesis I'm willing to accept the current thinking.

How about juvenile Accipiter poliogaster? Again barring new data or a better hypothesis, I can readily accept the suggestion that it mimics Ornate Hawk-Eagle to reduce the risk of predation / aggression from other raptors.

But a lot of cases get a lot fuzzier.

Even within Accipiters I think it's fascinating. Perhaps they all do mimic each other but does it even make sense that Goshawks or Cooper's Hawks would better tolerate another of their own species than a Sharp-shinned or Sparrowhawk? Or is it the case that there absolutely will be aggression but if the aggressor presumes the other bird to be an equal it will be an attempt to chase it off rather than kill it? Or is it related to other species in the ecosystem? Or are those just really good phenotypical traits that are well conserved?

Then the Yellowlegs are even harder to formulate a hypothesis for than Hairy/Downy or many other WP cases...
 
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Even within Accipiters I think it's fascinating. Perhaps they all do mimic each other but does it even make sense that Goshawks or Cooper's Hawks would better tolerate another of their own species than a Sharp-shinned or Sparrowhawk? Or is it the case that there absolutely will be aggression but if the aggressor presumes the other bird to be an equal it will be an attempt to chase it off rather than kill it? Or is it related to other species in the ecosystem? Or are those just really good phenotypical traits that are well conserved?
And then don't forget all those cuckoos mimicking Accipiters...
 
However, note from the abstract "Our empirical data thus offers no support for the strict Interspecific social dominance mimicry (ISDM) hypothesis as an explanation for downy–hairy woodpecker plumage convergence."

Leighton speculates that there may be mimicry in response to some third-party species... but what species would that be? What benefit does that confer on one or both species?

I don't dispute that there is some sort of convergence going on - but not all convergence is mimicry.
I have no horse in this race, but both of your questions are discussed at length by the authors in the paper (the complete text for which can be found on ResearchGate). I'll quote what is probably the most relevant passage below:

Another plausible explanation for the hairy–downy mimetic complex is deception of third parties, as hypothesized by Wallace (1869), later defined specifically as type-D disjunct defensive antergic mimicry (Rainey & Grether, 2007).

Indeed, we found some evidence for this hypothesis; downy woodpeckers held a nonsignificantly higher position in the dominance hierarchy than would be expected based on their body mass and phylogenetic position alone. These results demonstrate that downy woodpeckers win aggressive contests at a higher rate than expected (even after accounting for the tendency towards increased dominance in woodpeckers; see Miller et al., 2017a). Thus, species that are smaller-bodied and/or less aggressive than hairy woodpeckers (but of larger or comparable size to downy woodpeckers) are more likely to cede ground when challenged or chased by a downy woodpecker. This is similar to other cases of aggressive mimicry, where the mimic gains access to resources due to mimicry (Cheney, 2010, Nelson and Jackson, 2009).

We propose that reduced aggression from third-party species may be a more plausible hypothesis for avian mimicry than reduced aggression from the model. In general, competition is typically most intense between conspecifics (Anderson and Whiteman, 2015a, Anderson and Whiteman, 2015b, Hu and Tessier, 1995), and individuals typically need to identify conspecifics to breed successfully. Individuals should therefore be less prone to error when identifying conspecifics compared to identifying individuals of other species; it is therefore expected that hairy woodpeckers are adept at identifying whether or not another individual is a conspecific. Furthermore, vocalizations, well known species-recognition signs across birds, are given regularly by downy and hairy woodpeckers and are quite dissimilar (The Birds of North America, 2015). It is possible that other species besides hairy woodpeckers would be more readily fooled by hairy-mimicking downy woodpeckers, given the reduction in selective pressure to identify heterospecifics that are neither major predators, prey, nor close resource competitors. For example, downy woodpeckers often form flocks with white-breasted nuthatches, tufted titmice, Baeolophus bicolor, and black-capped chickadees, Poecile atricapillus. By occasionally fooling these nonmodel species into relinquishing resources (e.g. high-value invertebrates), the sum of these successful deceptions may provide the selective pressure that drives mimicry in this complex. Indeed, another study found that mimicking dangerous species can influence the feeding behaviour of target species. Specifically, Davies and Welbergen (2008) demonstrate that the Accipiter mimicry by Cuculinae cuckoos influences the behaviour of other sympatric species by depressing the feeding behaviour of smaller species.
 
In Europe, Great Spotted and Middle Spotted Woodpeckers look similar, and Lesser Spotted and White-backed looks similar, although their relatives are dissimilar looking woodpeckers. For example, Middle Spotted is a closer relative of the very different Yellow-crowned Woodpecker from India, to my great surprise.

Although it is not clear what is the reason of this mimicry. Woodpeckers are intolerant to others of their own species, so there is little obvious to be gained from mimicry. Woodpeckers are also common in the diet of predators, so the mimicry does not seem to provide protection from predators. It may be that the woodpeckers benefit from separating each other as not to compete. Much like unrelated waders with the same rump patterns benefit from flocking with each other.

Visual mimicry in birds is interesting. A mimicry of Long-eared Owl towards Eagle Owl in Eurasia and Great Horned Owl in North America is another example. Even more interestingly, in bat and plant relationship there are leaves designed to give good signal for echolocation. By extension, there can be such a thing that mammals which have poor eyesight have a mimicry of smells, which human biologists overlook because we ourselves have no sense of smell and did not bother to develop a science capable of studying it.
 
we ourselves have no sense of smell and did not bother to develop a science capable of studying it.
Humans have a very good sense of smell, broadly compatible to that of other mammals. An estimate I saw suggests we can distinguish a trillion different scents. Smell is not our dominant sense of course.

Many groups of birds look (broadly) the same and I think you need good and strong evidence to claim mimicry over other explanations for why this should be. Of course, the first thing to rule out is shared descent or phylogenetic constraints, but when you've done that you'd have to carefully unpick and remove the influence of (e.g.) similar habitat and lifestyle
 
I have no horse in this race, but both of your questions are discussed at length by the authors in the paper (the complete text for which can be found on ResearchGate). I'll quote what is probably the most relevant passage below:

I think I need to explain in more detail then.

In several of his writings, E.O. Wilson would demonstrate that what he called "Just So Stories" could be misused within evolutionary biology. In this usage, a "Just So Story" is a hypothetical explanation for some evolutionary phenomenon, but without empirical evidence or even critical analysis for or against it. Evolutionary biology is especially prone to this problem - not only does it suffer from the normal difficulties of biological research (e.g. few followup/secondary studies, observation issues, biases, etc. etc.) but there is a temporal-historic, environmental and generational component of evolution which cannot be replicated (e.g. even if you run generations of fruit flies, it will not be under the same conditions that fruit flies evolved; much less woodpeckers). So hypotheses and philosophical theories can have an inordinate amount of perceived explanatory power when they in fact do not. Or in other words, a story may be attractive because it seems to fit, but the bar is lower. "This makes sense" rather than "there is evidence for this" becomes more tolerable when finding evidence is more challenging. It is accepted because it is "just so."

The issue with Picidae plumage seems rife to me with "Just So Stories." Here we have a speculation that the "third party" species are all of nuthatches and Parids which form mixed flocks with Downy Woodpeckers... well, "often" and only in certain habitats, and much more rarely in places like California and New Mexico, but sure it happens. Not as much with Hairies, but that's a whole other criticism. From the study, "By occasionally fooling these nonmodel species into relinquishing resources (e.g. high-value invertebrates), the sum of these successful deceptions may provide the selective pressure that drives mimicry in this complex." The evidence of this? Cuckoos and Accipiters. But I missed the part where they demonstrate not only how this "occasional" behavioral occurrence is enough to drive the plumage difference of a species (or two). In this particular speculation, it is apparently proposed that Hairy Woodpeckers mimic Downies for some benefit - but I don't see it addressed as to why Dwony Woodpeckers have the pied plumage to begin with; what the benefit is to them and why a Hairy does not share the same benefit - their benefit is due instead to mimicry. But moreover, also missing is any demonstration that a resource differential actually occurs. In contrast to a lot of situations - there are easily testable components here: what happens when woodpeckers forage with vs. without chickadees, and what happens in those vast areas of the west and Mexico where there are no Downy Woodpeckers, but good populations of Hairy Woodpeckers (which strangely retain the plumage of the non-present species they are "mimicking...")

Watch how easy it is to produce a "Just So Story." There is good evidence to support the idea that zebras have black and white stripes because it confuses the horseflies which carry trypanosomal diseases. The flies have compound eyes and quirky vision, even for insects, and the pattern on the zebra's hide keeps them from effectively decelerating and landing on the animal for a blood meal. There are probably some sort of parasitic flies in North America which might attack woodpeckers - maybe those flies like the forests that Downy and Hairy Woodpeckers prefer. And chickadees too, and Black-and-White and breeding-season Blackpoll Warblers. Why, all of these species are mimicking... zebras. Nobody has disproven this hypothesis thus far - so we can treat it as if it is "just so." We could come up with dozens of these ideas - related to mimicry, or disease models, or habitat or predation or evolutionary history or even just to coincidence. All have the same explanatory power until there is empirical evidence to support or refute any of them. That step is what's apparently lacking in woodpecker mimicry.

So to be clear - the authors do not answer my questions, because empirical study is needed to answer my questions. Speculation just doesn't cut it. As I mentioned, this is a problem all around biology, but what fascinates me is that in this particular case of woodpecker plumage the story seems to have gained so much unearned strength, with so many weaknesses - and I can't exactly tease out why. Mimicry is valuable as a hypothesis, but only as a hypothesis. There needs to be much more rigorous testing before we rule out all the other potential reasons for plumage convergence.
 
That does make your position clearer, thank you for taking the time to elaborate. I don't speak for the authors, but I don't get the impression from their writing that they've presented the idea as anything more than a hypothesis (albeit one that they consider plausible based on circumstantial evidence), and I suspect they'd very much welcome more direct empirical testing of it.

The only thing I'd hasten to add is that the hypothesis posits downy woodpeckers benefit from resembling hairies instead of the other way around, so the fact that hairies retain the same color pattern in regions without downies would not seem to directly contradict it. And indeed, the hypothesis is not intended to explain why the color pattern evolved in the putative model species (in this case hairy woodpeckers) in the first place.
 
Possibly interesting is the fact that the Amami and Okinawa Woodpeckers, the sole woodpeckers on those islands, are basically partly and fully "non-pied" White-backed Woodpeckers; the isolated Arabian Woodpecker is a "non-pied" Middle Spotted Woodpecker (but still with black-and-white wings).
So there must be a benefit in not being pied there.
(In these cases it is logical to assume that the predecessors were indeed all pied).
 
The only thing I'd hasten to add is that the hypothesis posits downy woodpeckers benefit from resembling hairies instead of the other way around, so the fact that hairies retain the same color pattern in regions without downies would not seem to directly contradict it. And indeed, the hypothesis is not intended to explain why the color pattern evolved in the putative model species (in this case hairy woodpeckers) in the first place.
Ah, I think I was thrown off by their term "hairy-mimicking downy woodpeckers" and missing that crucial hyphen. It leads me to more head-scratching, however, as I believe the study found Downies to be (nonsignificantly) more aggressive than expected - so then their case for aggressive mimicry seems a bit backwards.
 

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