Visual mimicry of host nestlings by cuckoos

In this article, I will present the study “Visual mimicry of host nestlings by cuckoos” by Langmore et al. 2011. The biological model used here is the cuckoo, which is a brood parasite species. Brood parasites species lay their eggs in the nests of other birds and do not provide any parental care for their own offspring. This has a detrimental effect on the reproductive success of the hosts for several reasons. First of all, the parasite can evict the host offspring by removing host eggs from the nest, either the parasite female when it lays its eggs, or by the chick if it hatches earlier than the hosts chicks. Then, if the hosts chick stay alive, we will observe a diminution of the host nestling growth rate, because of a competition between the chicks for food and care. Because hosts are able to discriminate their offspring from the parasites offspring and then reject parasites' offspring, many brood parasites will try to increase the similarities between eggs and/or nestling parasites and their hosts' one to decrease the risk of rejection. With increasing fitness costs of parasitism, selection for host defenses increases, which in turn may force parasites to specialize and evolve fine-tuned adaptations that overcome a particular host’s defense. From brood parasitism results a coevolutionary arm race between hosts and parasites, and therefore a coevolution between them.

Coevolutionary mimicry in brood parasites is a counter-adaptation (i.e. result of coevolution between parasites and hosts) against host anti-parasitic response.

Here, we are going to focus on the visual part of mimicry of hosts nestlings by cuckoo parasites. Mimicry can be defined as an adaptation evolved by selection pressure from signal-receivers (Vane-Wright, 1980). It arises from a reciprocal interaction between two or more evolutionary lineages with each party selecting for changes in the other.

There are two types of brood parasitism, non-obligate and obligate. Non-obligate brood parasites lay eggs in the nest of conspecifics (i.e. same species) and in their own nests. Obligate brood parasites lay eggs in nests of other species and have completely lost the ability to construct nests and incubate eggs.

The three parasites species study here are Chalcites bronze-cuckoos, and their respective hosts. They are obligate brood parasites. The hypothesis tested here is whether the evolution of cuckoo chick discrimination by hosts of Australian bronze-cuckoos has reciprocally selected visual mimicry of host young by cuckoos sensory systems. The particularity of this study is the use of supposed bird criteria to assess the resemblance between hosts nestlings and parasites.

Methods

The species of bronze-cuckoos and their hosts studied were :

- Horsfield’s bronze- cuckoo C. basalis (primarily parasitizes Malurus hosts)

- Shining bronze-cuckoo C. lucidus plagosus (primarily parasitizes Acanthiza hosts)

- Little bronze-cuckoo C. minutillus (primarily parasitizes Gerygone hosts).

The study was conducted in Australia, at one site for every species but C. minitillus, studied at two sites, with two subspecies parasites of the same host.

After the location of the nests either by following adults or by searching for nests (for Gerygone nests), some of them were protected with a cage to avoid the predation by large predators, to minimize loss of data.

Spectral reflectance of nestlings' skin was measured (back and flange), and the nest irradiance spectra calculated.

Then, they analyzed the volume of avian color space that every individuals occupied, in order to calculate the level of color variation among and within the cuckoos and hosts. The more volume is occupied, the more variation there is.

The next step was a visual modeling to predict if a bird would be able to discriminate between two objects based on color (chromatic variation) or luminance (perceived lightness). I won't detailed the statistical analysis here.

Results

Chalcites cuckoo nestlings show substantial appearance variation between cuckoo species, but resemble strongly to their respective hosts. Especially, the variation in skin color was greater between cuckoo species than between cuckoo-host.

Figure 1. Representative photographs and mean+s.e. reflectance of the skin of nestling bronze-cuckoos (blue lines) and their hosts (pink lines). (a) Little bronze-cuckoo and large-billed gerygone. (b) Shining bronze-cuckoo and yellow-rumped thornbill . (c) Horsfield’s bronze-cuckoo and superb fairy-wren (n ¼ 17). (d) We also include a second host of Horsfield’s bronze-cuckoo, the purple-crowned fairy-wren M. coronatus

The visual modeling was used to assess if the nestling cuckoo was a better visual mimicry of its own host other host species. They found that the level of match between the appearance (skin color and luminance) of the nestling cuckoo and its host was correlated with the degree of host specificity :

- Little bronze-cuckoo almost perfect match with its host (specialist parasite of darkskinned gerygone hosts), an is significantly different from other hosts

- Shining bronze-cuckoo show significantly more similarity to both thornbill and fairy-wren hosts than to gergyone hosts. Intermediate host specificity parasites both thornbill and fairy-wren hosts (secondarily)

- Horsfield’s bronze-cuckoo present a similar degree of resemblance for every hosts. Specialized on fairy-wrens throughout its range, but secondarily exploit a range of other hosts.

- The rictal flange color of nestling bronze-cuckoos was more similar to their primary hosts than to non-hosts for all three cuckoo species.

- The rictal flange luminance shows no correlation between parasites and hosts for any cuckoo species.

Figure 2. The disparity (mean+s.e.) between bronze-cuckoos and their own hosts versus other hosts in (a,d,g) skin colour, (b,e,h) skin luminance and (c,f,i) rictal flange colour. (a–c) Little bronze-cuckoo; (d–f ) shining bronze-cuckoo; (g–i) Hors- field’s bronze-cuckoo. SFW, superb fairy-wren; YRT, yellow-rumped thornbill; LBG, large-billed gerygone. The arrow indicates the primary host in each graph. The asterisks indicate Tukey HSD significance levels (p, 0.05) with the bars below indicating the two species being compared.

Discussion

These results show the evidence of a visual mimicry to host young by cuckoo nestlings for the first time. Indeed, the experiments, by using a “bird point of view” and not only similarities in the appearance for human eyes makes this study different.

However, we need to make sure that the similarities observed are indeed coevolution in response to discrimination by hosts and not “simple” similarities. The necessity of making this distinction was pointed out by Grim in 2004 in his study “Mimicry vs. similarity: which resemblances between brood parasites and their hosts are mimetic and which are not?”. To be called “mimicry”, a similarity should be the result of a coadaptation, otherwise the similarity is cryptic (non-mimetic), and results from convergent evolution (Harrison, 1968; Mason & Rothstein, 1987). So we need to assess if the similarities are specific adaptations and counteradaptations, (2) adaptations resulting from other (non- coevolutionary) selection pressures, or just (3) by- products of some other – perhaps adaptive – traits.

Several processes might create similarities between hosts and parasites, and they are the same eggs similarities and nestling similarities (Grim 2004) :

1. Phylogenetic constraints : the similarity of egg and chick appearance is probably the result of common descent. This process is applicable for intra-specific parasitism.

2. Random matching : if the parasites have a large range of hosts. For example with passerines, which show limited inter-specific variation in the appearance of their eggs.

3. Spatial autocorrelation in the diet of hosts and parasites : environmental similarities could influence the coloration of both host and parasite eggs in the same way. This hypothesis is only applicable for eggs.

4. Nest predation : predation could select for an inconspicuous appearance in both host and parasite eggs and nestling (no evidence shown for nestling, but applicable in theory)

5. Egg replacement by competing female cuckoos : in this case the model is the host’s egg, the mimic is the egg of the first cuckoo and the operator is the second-arriving cuckoo.

6. Host discrimination : increase similarities with hosts eggs and chicks to avoid rejection.

Clearly, 1, 2 and 3 have nothing to do with coevolution, process 4 is crypsis, and only 5 and 6 are examples of mimicry.

The coevolution between Chalcites cuckoos and their hosts almost certainly has selected for mimicry of host nestlings by cuckoos because experimental studies show that (1) hosts of Chalcites cuckoos can reject parasite nestlings (2) chick rejection is a specific response to brood-parasitism, such that hosts show flexibility in their responses to nestlings depending on the risk of parasitism; and (3) non-mimetic nestlings suffer a survival cost. These results were found in previous study by Langmore et al. (2003, 2009).

As a conclusion, we can say that visual mimicry is a result of the evolutionary arm race between brood-parasites and their hosts, and that the degree of specialization of the parasite is correlated with the level of resemblance with the hosts.

Citations



[1] N. B. Davies and J. a Welbergen, “Cuckoo-hawk mimicry? An experimental test.,” Proceedings. Biological sciences / The Royal Society, vol. 275, no. 1644, pp. 1817-22, Aug. 2008.

[2] Davies and Brooke, “AN EXPERIMENTAL STUDY OF CO-EVOLUTION BETWEEN THE CUCKOO , CUCULUS CANORUS , AND ITS HOSTS . AND GENERAL DISCUSSION,” Journal of Animal Ecology, 1989.

[3] T. Grim, “Mimicry vs . similarity : which resemblances between brood parasites and their hosts are mimetic and which are not ?,” Society, pp. 69-78, 2005.

[4] O. Krüger, “Brood parasitism selects for no defence in a cuckoo host.,” Proceedings. Biological sciences / The Royal Society, no. February, Feb. 2011.

[5] N. E. Langmore, G. Maurer, G. J. Adcock, and R. M. Kilner, “Socially acquired host-specific mimicry and the evolution of host races in Horsfield’s bronze-cuckoo Chalcites basalis.,” Evolution; international journal of organic evolution, vol. 62, no. 7, pp. 1689-99, Jul. 2008.

[6] N. E. Langmore et al., “Visual mimicry of host nestlings by cuckoos.,” Proceedings. Biological sciences / The Royal Society, vol. 278, no. 1717, pp. 2455-63, Aug. 2011.