Over at Nothing in Biology Makes Sense!, Amy Dapper discusses a new study of brood parasites, birds that lay their eggs in the nests of other bird species, letting those adoptive hosts take on the costs of raising the brood parasites’ chicks. This sounds like a bad deal for the host species, but in at least one case, it turns out that a brood parasite chick can be a boon to its adoptive nest-mates:
Canestrari et al. (2014) focused on the great spotted cuckoo (Clamator glandarius) and their host, carrion crows (Corvus corone corone). They studied the success rate of nests with and without brood parasitism and found that carrion crow nests that contained parasitic cuckoo nestlings were actually more likely to be successful (i.e. fledge at least one crow nestling). How could this be?
Brood parasitism, the reproductive strategy of choice for cuckoos and cowbirds, sounds like a lazy approach to parenting: lay your eggs in another bird’s nest, and let the unwilling adoptive parents take the trouble to raise your chicks. But contracting out parental care like this comes with many of its own complications. Chicks raised by parents of a different species have to eliminate competition from their adoptive nestmates, and may grow up a bit confused; reluctant host birds may need to be told, and reminded, that raising cuckoo chicks is an offer they can’t refuse.
But before crossing all those hurdles, a brood parasite’s first task is to lay eggs in the nest of a host who won’t immediately recognize and reject them. The strong natural selection imposed by host rejection has led cuckoos to evolve “host races” that lay eggs whose color and spotting pattern matched to those of their preferred host species. This kind of broad-scale pattern could arise without much direct effort by female cuckoos—those who lay eggs in the nest of the best matching host species would simply be the ones most likely to have chicks that survive to the next generation. But is it possible that cuckoos do take an active role in matching up to their hosts, seeking out host nests containing eggs that look like their own?
The answer, according to a series of studies over the last several years, is yes—probably.
Cuckoo eggs (indicated by arrows) in the nests of three different host species. Illustration via The Knowledge Project.
Although the match between cuckoos’ eggs and those of the specific host species whose nests they invade is striking even to human eyes, it had been generally assumed that, within these egg-matching associations, cuckoos could choose nests pretty much at random. That is to say, while the differences in coloration and spotting between the eggs of different host species were enough to make it hard for a cuckoo egg to blend in with the nests of redstarts and warblers at the same time, a cuckoo whose eggs match the eggs of one redstart will also match the eggs of most other redstarts.
A 2006 study suggested this thinking might be wrong. A group of European ornithologists took advantage of a handy “natural experiment” on the Dutch island of Zealand, where cuckoos had been absent until the early twentieth century. Using museum specimens of cuckoo eggs and eggs from the reed warbler nests in which they were collected, the team compared the match between cuckoo egg color and host egg color over time. Improved matching could be due to female cuckoos selecting better-matched host nests in the new host population; but it could also be created by simple natural selection—the colonizing cuckoos evolving eggs that better matched the host population on average. The coauthors found evidence of rapidly improved matching—but no evidence that the cuckoo’s egg color had changed overall. It looked like the newly arrived brood parasites were adapting by learning, or by evolving, preference for better matches.
Some of the same ornithologists followed this result with a small 2007 study that more directly examined the role of host choice by cuckoos. At a field site in Hungary, they measured the match between cuckoo eggs laid in the nests of great reed warblers, and compared the rate at which warbler parents ejected the naturally-laid cuckoo eggs to the rate at which they rejected randomly-drawn cuckoo eggs introduced into their nests by members of the research team. They found that, indeed, the cuckoo-laid cuckoo eggs were better matches to the eggs in their host nests than researcher-laid cuckoo eggs were—and, more importantly, warblers were less likely to reject the better-matched cuckoo-laid eggs.
A great reed warbler is probably ready for this cuckoo chick to leave the nest. Photo by phenolog.
This result was somewhat complicated, however, by a study just published in PLoS ONE. This time the authors, again including many of the same ornithologists involved in the original 2006 study, compared the match between cuckoo eggs laid in marsh warbler nests at a site in Bulgaria to the cuckoo eggs’ potential match with warbler eggs in nearby unparasitized nests.
If cuckoos were choosing the best-matched host nests, the authors reasoned, there should be a better match between cuckoo eggs and the eggs in parasitized nests than in nearby nests, which the same cuckoo could have used, but didn’t. Six years after the original cuckoo choosiness study, the team was able to use a new approach to compare the match between host and cuckoo eggs: rather than simply compare the spectrum of light reflected by the eggs, they fed the measured spectrum into a mathematical model of bird vision—an approach used in other studies of brood parasites, which is thought to be superior because it estimates how similar, or different, two eggs look through the eyes of a host parent.
With this approach, the team found that cuckoo eggs were not siginificantly better matched to warbler eggs in parasitized nests than they were to eggs in nearby unparasitized nests. Did this overturn the previous evidence for choosy parasitic parents? Well, maybe.
On the one hand, the new study uses the new vision model comparison method, which should give more biologically meaningful results. But on the other, the new study’s design is different in from the 2007 study in a critical way: it doesn’t tell us whether cuckoos’ host choices make the hosts less likely to reject cuckoo eggs. In the 2007 study, there was no need to guess whether the statistical comparison of egg color spectra was biologically meaningful—host parents “told” the researchers that the comparison mattered by rejecting randomly-chosen cuckoo eggs more often than they did eggs laid by actual cuckoos.
So, although there are good reasons to think that the form of measurement used in the new study is better, it’s not clear to me that the result is actually more useful for understanding how natural selection could be acting on cuckoos choosing among many available host nests in a single population. What I’d like to see is a study using the field methods of the 2006 study, and the color matching methods of the 2012 one. ◼
Antonov, A., Stokke, B., Fossøy, F., Ranke, P., Liang, W., Yang, C., Moksnes, A., Shykoff, J., & Røskaft, E. (2012). Are cuckoos maximizing egg mimicry by selecting host individuals with better matching egg phenotypes? PLoS ONE, 7 (2) DOI: 10.1371/journal.pone.0031704
Avilés, J., Stokke, B., Moksnes, A., Røskaft, E., Åsmul, M., & Møller, A. (2006). Rapid increase in cuckoo egg matching in a recently parasitized reed warbler population Journal of Evolutionary Biology, 19 (6), 1901-10 DOI: 10.1111/j.1420-9101.2006.01166.x
Cherry, M., Bennett, A., & Moskat, C. (2007). Do cuckoos choose nests of great reed warblers on the basis of host egg appearance? Journal of Evolutionary Biology, 20 (3), 1218-22 DOI: 10.1111/j.1420-9101.2007.01308.x
The brood parasite in question is the greater honeyguide, an African bird best known for helping people find bee colonies (though the story that honeyguides also guide honey badgers don’t have much factual basis). However, honeyguide females also lay their eggs in the nests of several host species—including hoopoes, greater scimitarbills, green woodhoopoes, little bee-eaters, and striped kingfishers. Although the honeyguides’ eggs aren’t colored like their hosts’, they do have matching shapes—the hosts all nest in tree cavities, where lighting is too poor to notice a mis-colored egg, but an oversized or oddly shaped one would stand out.
A hoopoe, one of the birds that “adopts” greater honeyguide eggs. Photo by Hiyashi Haka.
There’s an evolutionary catch, though: hoopoes, scimitarbills, and woodhoopoes lay oblong eggs, while the bee-eaters and kingfishers lay spherical eggs. Yet honeyguide females manage to lay eggs of matching shape and size in the nest of each host. Individual brood parasites can’t adjust the shapes of their eggs to match those in a host nest—they find hosts with eggs that will match their own.
How do they do it? Maybe each female honeyguide actually goes looking for nests like the one she grew up in, either because she is compelled to by some genetic instinct, or because she learns to recognize a potential host in the course of being raised by that host. Or maybe the host birds are so good at recognizing and rejecting oddly-shaped parasite eggs that only well-matched eggs make it to adulthood. Any of these processes could result in long lineages of female honeyguides laying eggs in the nests of the same host species their mothers, grandmothers, and great-grandmothers used. This is precisely the pattern Claire Spottiswoode and her coauthors found in the population genetics of greater honeyguides.
Spottiswoode et al. collected genetic data from honeyguides using all five of the host species mentioned above, and compared the patterns of relatedness from different genetic markers to patterns of host use. The pattern of differentiation in a marker from the mitochondrial genome—genes contained in the mitochondria, which mothers pass on to their offspring but fathers do not—neatly divides the honeyguides between hosts with oblong eggs and the hosts with spherical eggs. By applying a molecular clock to the mitochondrial data, the team found that the division between oblong-egg and spherical-egg honeyguides dates back as long as 3 million years ago. So honeyguide females have been tracking the same hosts, or very similar ones, for quite some time!
However, no such pattern is evident in four genetic markers from the nuclear genome, which is inherited via both parents. That suggests male honeyguides don’t discriminate among females based on host fidelity—mates pair off regardless of what host species they each grew up with. Spottiswoode et al. also note that this result hints at how honeyguide egg characteristics and host preferences could be inherited: via the female sex chromosome. In birds, biological sex is determined by the Z and W chromosomes—individuals with two Z chromosomes develop as males, and individuals with a Z and a W chromosome develop as females. Host preferences and egg shape inherited via the W chromosome would then be carried only by females.
However, the data presented here don’t directly test the W-chromosome hypothesis. That would require markers—or better yet complete sequence data—from the W chromosome itself, and (to be really thorough) lots more markers from the rest of the nuclear genome as well. That’s a lot of genetic data to collect, but we are very close to the day when such data are easily collectible. ◼
Spottiswoode, C., Stryjewski, K., Quader, S., Colebrook-Robjent, J., & Sorenson, M. (2011). Ancient host specificity within a single species of brood parasitic bird. Proc. Nat. Acad. Sciences USA, 108 (43), 17738-42 DOI: 10.1073/pnas.1109630108
The common cuckoo is such a lazy parent that brood parasitism—laying its eggs in the nests of other birds—is built into its biology.
No bird will willingly adopt cuckoo chicks, which usually out-compete, and sometimes kill, their adoptive siblings. Given any hint that one of the eggs in her nest isn’t hers, a bird will eject the intruder. So cuckoos have evolved eggs that mimic the coloring of their hosts’ eggs—dividing the species into “host races” that specialize on a single host species, and lay eggs that mimic that host’s.
Cuckoo eggs (indicated by arrows) in the nests of three different host species. Illustration via The Knowledge Project.
Birds see the world differently than humans—where we have three kinds of color-sensitive cells in our eyes, they have four. This allows them to see colors in the ultraviolet range, which is invisible to us. Birds’ eyes also have an additional class of sensory cell that may help them perceive and discriminate among textures. So to study the match between cuckoo and host eggs, Stoddard and Stevens first had to figure out what each egg looked like to a bird.
A reed warbler feeds the cuckoo chick that has taken over its nest. Photo via Wikimedia Commons.
To do this, they developed a mathematical model of each host species’ vision. The model estimated how similar two eggs should look to a bird, given raw data about what colors of light the eggs reflect and the specific colors the bird can detect. Using the model, Stoddard and Stevens could then calculate the “overlap” between the colors and patterning of a host egg and the egg of a cuckoo specializing on that host species.
Stoddard and Stevens then applied the vision model’s measure of similarity to museum specimens of eggs from the cuckoo-parasitized nests of eleven European bird species. They found that cuckoo eggs matched their hosts’ quite well overall, but the match was best for cuckoos specialized on especially vigilant hosts. For each host, the authors looked up studies of egg rejection behaviors to calculate the probability that each species would eject eggs that didn’t look like their own. Species with higher ejection probabilities were parasitized by cuckoo host races whose eggs were better mimics.
If you’re a bird, brood parasitism seems like a cushy reproductive strategy—lay your eggs in someone else’s nest, then sit back and let the inadvertent foster parents raise your kids for you. But what if they don’t raise you kids quite right? Could brood parasite chicks raised by parents of another species grow up a bit … confused? According to a recent study of brood-parasitic ducks, they can indeed [$a].
Redheads (above) sometimes lay eggs in the nests of canvasback ducks (below)—but redhead chicks raised by canvasbacks may not know what species they are. Photos by Nick Chill and meantux.
The new study examines redheads, a species of North American duck which frequently lays its eggs in the nests of other duck species, particularly the canvasback duck, which occupies much of the same range. Redheads are facultative brood parasites—in years when conditions produce lots of resources, female redheads lay eggs in other ducks’ nests as a supplement to their own nests; and in poorer years, they may lay only parasitic eggs [PDF]. Canvasback ducks, on the other hand, will lay eggs in the nests of other canvasbacks (which is not uncommon in birds [$a]), but don’t parasitize other species.
This sets up a nice behavioral experiment. In birds, species recognition may be due to varying degrees of nature and nurture—a male bird may recognize females of his own species by genetically-transmitted instinct, but he may also have to learn socially important songs or other behaviors from his parents and other adults. You might expect that redhead chicks have evolved to recognize their own species regardless of who raised them, while canvasbacks might be confused if they grow up around another species. So the authors experimentally transferred just-hatched male redhead chicks into canvasback broods, and male canvasback chicks into redhead broods, and compared their social development to male chicks raised by their own species.
A female redhead spurns the advances of a cross-fostered male canvasback. Photo from Sorenson et al. (2010), figure 2.
When the chicks had grown up, the authors offered the cross-fostered males access to females of both species, and recorded their interactions. It turned out that the brood parasitic rednecks were just as prone to species-confusion as the canvasbacks. Males of both species preferred to associate with females of the species with which they were raised, and directed almost all of their courting effort—displays of neck-arching and special calls—toward the species that fostered them. In fact, many of the cross-fostered males successfully formed mated pairs with females of the other species.
So why hasn’t redhead parasitism of canvasback nests broken down the reproductive isolation between these two species? The authors don’t have a clear answer, but note that the rate of observed hybrid couplings are much lower in natural populations than in their experimental setting. Social learning is a complicated thing, and life in larger, natural populations of the two species might not be well replicated in this study.
Petrie, M., & Moller, A. (1991). Laying eggs in others’ nests: Intraspecific brood parasitism in birds. Trends in Ecology & Evolution, 6 (10), 315-20 DOI: 10.1016/0169-5347(91)90038-Y
Sorenson, M., Hauber, M., & Derrickson, S. (2010). Sexual imprinting misguides species recognition in a facultative interspecific brood parasite. Proc. Royal Soc. B, 277 (1697), 3079-85 DOI: 10.1098/rspb.2010.0592
Sorenson, M. (1991). The functional significance of parasitic egg laying and typical nesting in redhead ducks: an analysis of individual behaviour. Animal Behaviour, 42 (5), 771-96 DOI: 10.1016/S0003-3472(05)80122-8
Brood parasitism, in which one bird species lays its eggs in another bird’s nest, has long been considered a likely cause of coevolution [$a] between brood parasites and their hosts, because the interaction exerts strong natural selection on both species. Hosts suffer major fitness consequences if they take on the raising of another bird’s chick—and brood parasite chicks are often bigger, and more aggressive, than their adoptive “siblings,” sometimes pushing them right out of the nest. On the other hand, brood parasites run the risk of losing their offspring to hosts who can recognize a strange egg and eject it from the nest. One way to avoid raising a cuckoo chick is to lay eggs that look different from cuckoo eggs. Cuckoos counteract this defense by evolving eggs that match their most common hosts—a selective regime proposed to explain rapid rates of species formation in parasitic cuckoo lineages. In the new study, Yang et al. show that this pattern plays out within a single population of ashy-throated parrotbills and the cuckoos that parasitize them. At a forested nature reserve in southwestern China, the team found that parrotbills lay eggs of three different colors: white, blue, or (rarely) pale blue. Common cuckoos in the same area also laid eggs of those three colors, in about the same proportions as the parrotbills—and cuckoo eggs were usually found in host nests with eggs of the same color. Experimental introduction of eggs into parrotbill nests confirmed that parrotbills were more likely to reject eggs colored differently from their own.
That result captures many of the necessary conditions for coevolution between ashy-throated parrotbills and the local cuckoo population; the frequency with which parrotbills reject eggs unlike their own should exert strong selection on the cuckoos, and (conversely) the frequency with which parrotbills fail to reject cuckoo eggs that look like their own should exert selection on the hosts. This isn’t the first case in which brood parasites have apparently forced their hosts to diversify, however—notably, African village weaverbirds evolved less varied egg patterning after being introduced into parasite-free habitats on Mauritius and Hispaniola.
Krüger, O., Sorenson, M., & Davies, N. (2009). Does coevolution promote species richness in parasitic cuckoos? Proc. Royal Soc. B, 276 (1674), 3871-9 DOI: 10.1098/rspb.2009.1142
Lahti, D. (2005). Evolution of bird eggs in the absence of cuckoo parasitism. Proc. Nat. Acad. Sci. USA, 102 (50), 18057-62 DOI: 10.1073/pnas.0508930102
Yang, C., Liang, W., Cai, Y., Shi, S., Takasu, F., Møller, A., Antonov, A., Fossøy, F., Moksnes, A., Røskaft, E., & Stokke, B. (2010). Coevolution in action: Disruptive selection on egg colour in an avian brood parasite and its host. PLoS ONE, 5 (5) DOI: 10.1371/journal.pone.0010816
Among birds, brood parasites are the ultimate freeloaders — species like the common cuckoo and the brown-headed cowbird lay their eggs in other birds’ nests, leaving the host to raise the parasite chicks at the expense of its own. But while brood parasitism is easy on the parents, it isn’t so easy on their chicks, as a study recently published in PLoS ONE suggests.
A brood parasitic chick faces two challenges. The first is to avoid being recognized by its adoptive parents and ejected from the nest; the second is to win parental attention in competition with their adoptive nest-mates. The first challenge may be partially met by the evolution of eggshells that match host eggshells; and brood parasite parents may also help by keeping watch on the host nest so they can punsish hosts who eject introduced eggs. (This punishment behavior has been described as an “avian mafia [$-a].”)
In competition with their adoptive nest-mates, though, parasitic chicks are on their own. If the host’s own eggs hatch, the host has more mouths to feed and less time to spend on the parasitic chick. On the other hand, a brood parasitic mother can’t kick out the host’s eggs at the time she leaves her own egg with the host, because the host may abandon a nest that contains only a single unfamiliar-looking egg. This leaves it to freshly-hatched brood parasite chicks to do the heavy lifting involved in ejecting their host’s eggs themselves.
A common cuckoo chick pushes one of its host’s eggs out of the nest. Detail of figure 1 from Anderson et al. (2009).
Egg eviction looks like hard work — the chicks attempt it while they’re not much bigger than the eggs. Anderson et al. investigated the cost of all this adoptive-siblicidal effort by manipulating reed warbler nests that had been parasitized by common cuckoos,* taking away the hosts’ eggs in experimental nests, and comparing the growth of cuckoo chicks in those nests to that of chicks in unmanipulated nests, who had to do the evicting themselves.
They found that there is a cost to eviction effort: during the period of development when they would be doing all they could to push eggs out of the nest, cuckoo chicks grew faster when they didn’t have eggs to push. But they didn’t grow much faster, and by the time they were ready to leave the nest, the advantage had disappeared. Anderson et al. take this to mean that the cost of eviction is “recoverable” through the benefits of increased parental attention later on. I would add that it points out how important your choice of time frame can be when investigating how traits or behaviors affect organisms’ evolutionary fitness — sometimes a cost paid at one point in development is an investment toward later benefits.
——– *The common cuckoo is the species first known to parasitize other birds’ nests, and its name is the linguistic source of the term “cuckold.”
Anderson, M., Moskát, C., Bán, M., Grim, T., Cassey, P., & Hauber, M. (2009). Egg eviction imposes a recoverable cost of virulence in chicks of a brood parasite. PLoS ONE, 4 (11) DOI: 10.1371/journal.pone.0007725
Hoover, J., & Robinson, S. (2007). Retaliatory mafia behavior by a parasitic cowbird favors host acceptance of parasitic eggs. Proc. Nat. Acad. Sci. USA, 104 (11), 4479-83 DOI: 10.1073/pnas.0609710104
Lahti, D. (2005). Evolution of bird eggs in the absence of cuckoo parasitism. Proceedings of the National Academy of Sciences, 102 (50), 18057-62 DOI: 10.1073/pnas.0508930102
Soler, M., Soler, J., Martinez, J., & Moller, A. (1995). Magpie host manipulation by great spotted cuckoos: Evidence for an avian mafia? Evolution, 49 (4), 770-5 DOI: 10.2307/2410329