Scientists crack the egg, the evolutionary puzzle

Cuckoo sparrow eggs are laid by different females. Diversity of maternally inherited egg phenotypes within a single crossbreed, the cuckoo finch brood parasite. Different cuckoo sparrow matrilines mimic the eggs of different host species (here, the brown-winged terrier and the red-faced cisticola) and have diversified further to approximate the range of variable egg “signatures” within each host species, an antiparasitic adaptation that helps host parents identify their eggs. Credit: Claire N. Spotswood

As many humans prepare to unpack the Easter eggs, scientists have managed to solve one of nature’s biggest criminal cases, the two-million-year-old egg fraud scandal. Their findings suggest that the victims of this fraud may now have the upper hand.

Worldwide, many birds avoid the costs of parenthood by laying their eggs in the nest of other species. This lifestyle, called “brood parasitism,” has many advantages but also presents challenges such as how to persuade other species to accept an alien egg. Many brood parasites achieve this by mimicking the colors and patterns of their host’s eggs, but some take advantage of the care of so many different host species whose eggs all look different.

How then can one type of parasitic brood mimic the eggs of many different bird species to trick them into raising their young? And how do these parasitic fakers pass this ability to their young despite interbreeding between birds raised by different hosts?

These questions have baffled scholars for more than a century. Now genetic research by an international team led by Professor Claire Spottiswood from the Department of Zoology at the University of Cambridge and the Fitzpatrick Institute of African Ornithology at the University of Cape Town; And Professor Michael Sorenson at Boston University, they’ve made significant progress, and their findings may be bad news for egg forgers.

The study, published today in PNAS, focusing on the genetics of egg mimicry in the cuckoo, a species that adopts a parasitic brood lifestyle and exploits several species of warbler across Africa. The research reveals that female cuckoo finches inherit their ability to mimic the appearance of their host’s eggs from their mothers, via the female’s W chromosome (similar to the male’s Y chromosome in humans).

Scientists crack the egg, the evolutionary puzzle

Cuckoo sparrow and host chicks. Brood parasitism is costly to the hosts because the cuckoo sparrow chick is aggressively begging for food once they hatch, outperforming the chicks of the host parents (here zitting cisticolas) that usually die of starvation soon. Credit: Claire N. Spotswood

This ‘maternal inheritance’ allows cuckoo finches to overcome the risk of inheriting faulty mimicry genes from a father raised by a different host, thus allowing distinct lineages of female cuckoo finches to develop specialized egg mimics for many different host species. Such a tradition tricks host parents into accepting a parasitic egg as their own rather than throwing it out of the nest, and thus has been crucial to the success of these African birds.

But the researchers believe that this well-established “genetic structure” of maternal inheritance may come back to haunt the cuckoos. Dr Spottiswood said: “In the inter-species evolutionary arms race, natural selection has created a double-edged sword.

“While maternal genetics has allowed cuckoo finches to exploit multiple host species, it is likely to slow their ability to develop counter-adaptations as their hosts develop new defences. In particular, parasites face a formidable challenge because some host species have in turn evolved an astonishing diversity of color eggs and ‘pattern signatures’ that help hosts distinguish their eggs from parasitic imitators”.

Field data were collected at a study site in southern Zambia with Dr Winvi Tong and Dr Gabriel Jimmy from the University of Cambridge, Ailsa Green, Selki Hammama, Ian Taylor and Collins Moya from the surrounding community in Zambia. The cuckoo sparrows in this area trick four different species of weedbird to devastating effect: If the host parents fail to detect and remove a parasitic egg in their nest, the young cuckoo sparrow will usually outgrow its host’s chicks, which soon starve to death.

The team collected DNA samples from 196 cuckoo birds from 141 nests belonging to four species of grasshopper birds and studied the majority by sequencing thousands of short segments across their genomes.

Scientists crack the egg, the evolutionary puzzle

A yellow-bellied empress, a common species of cuckoo sparrow, was captured in Zambia for genetic sampling with the help of field assistant Tom Hamosekele. Credit: Claire N. Spotswood

In their fight against counterfeiters, weedbirds have become skilled quality-checkers, rejecting eggs that differ from their color and pattern, and all four species have evolved the ability to deposit unique “signatures” on their eggs to enhance their detection from intruders. For example, prinias surrounded by yellow, lay eggs with blue, white, red or olive green backgrounds covered with a variety of patterns.

Cuckoo finches responded not only by mimicking the eggs of several host species, but also diversified to mimic at least some of the imprint-like variation seen in the eggs of different females within each host species. The team established that both abilities are passed down through maternal inheritance, and finally validated a hypothesis first proposed in 1933 by ornithologists who ponder how the common European cuckoo was similarly able to mimic the eggs of many different host species.

Counterfeiters who face an uncertain future?

Researchers believe that cuckoo finches now face an uphill struggle because they cannot re-incorporate the various forgery traits that evolved from their separate family lineages. For example, two different lineages of cuckoo sparrow mothers have developed eggs with blue or red backgrounds, as an evolutionary response to similar diversity in their brown-winged hosts, but there is no evidence that they can produce the exact mixture of pigments required to produce the olive green eggs that female host females can produce. .

In an earlier study, Professor Spottiswoode found that an increasing proportion of eggs laid by brown-winged Prinia hosts are olive green, suggesting that this is part of an accelerating evolutionary fight. As expected, the team found that these host birds pass on their anti-fraud capabilities to “egg-sign” through a different genetic process (two-parent inheritance) to that used by cuckoo finches.

Scientists crack the egg, the evolutionary puzzle

Cuckoo sparrow eggs in a zitting cisticola nest. Cuckoo sparrow eggs closely mimic the color and pattern of eggs of each of its multiple host species, to trick the host parents into accepting the parasitic egg as one of their own. Here a cuckoo bird successfully accepts its egg (left) into a nest of zitting cisticola (egg on the right). Credit: Claire N. Spotswood

Spottiswoode said: “Cuckoo finches lack a powerful source of evolutionary novelty and that could be costly in this ongoing arms race. The way they inherit their ability to mimic the host’s eggs has a downside by making the grasshopper’s defenses more effective, limiting the parasite’s ability to respond. .

“We may be seeing the emergence of non-falsifiable egg signatures that can force cuckoo finches to switch to other naïve host species. Or parasitic birds may become increasingly dependent on young host individuals who have not yet learned their own signatures and are bad at spotting an egg mismatch.”

The study argues that “selection from host defenses prompted cuckoo finches to transfer control of egg appearance to the inherited portion of the maternal genome” at least two million years ago.

Deceitful birds mimic their host young to deceive adoptive parents

more information:
The genetic architecture facilitates and then constrains adaptation in the co-evolutionary arms race between a host-parasite, Proceedings of the National Academy of Sciences (2022). DOI: 10.1073/pnas.2121752119

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