Female kākāpō and chick
The flightless kākāpō of New Zealand, a critically endangered member of the parrot family comes in two colour forms - olive and green - and neither seems to convey any obvious advantage over the other.
As an example of intelligent [sic] design, this would be an example of muddle and incompetence since, no matter how slight, one colour form would be better than the other so there would be no point in having two. It might be easier to manufacture one set of pigments for example, and having the ability to produce two different color forms with variants of the same genome when there is no advantage of one over the other is an unnecessary complexity of which any half-decent intelligent designer would be ashamed.
But as an example of what evolution by natural selection can produce, it makes perfect sense, especially when whatever environmental selectors produced the two colour forms might not now exist, so the cause might not now be obvious to a casual observer, unaware of the historical environment in which these traits evolved.
Please tell me all about the New Zealand flightless parrot, the kākāpō and what's known of its evolution. The kākāpō (pronounced kaah-kaah-po), scientifically known as Strigops habroptilus, is a unique and critically endangered flightless parrot native to New Zealand. Here's an in-depth look at this fascinating bird, including its natural history, evolutionary background, and conservation status.Now Lara Urban at Helmholtz AI, Germany and colleagues from the Aotearoa New Zealand Department of Conservation and the Māori iwi Ngāi Tahu, have worked out that these colour forms my have evolved in response to selection pressure provided by extinct apex predator birds.
- Physical Characteristics
- Flightless: The kākāpō is the world's heaviest parrot, weighing between 2-4 kg (4.4-8.8 lbs). Due to its weight and body structure, it cannot fly.
- Nocturnal: It is primarily active at night, and its mottled greenish-yellow feathers provide excellent camouflage among forest vegetation.
- Owl-like Face: Its name means "night parrot" in Māori, and it has a distinctive owl-like facial disc of feathers that helps with its acute sense of smell.
- Herbivorous Diet: The kākāpō feeds mostly on leaves, seeds, fruits, and roots, with a particular fondness for the native rimu fruit.
- Behavior
- Ground-Dwelling: Being flightless, it walks or climbs trees using its strong legs and sharp claws. Instead of flying, it glides or parachutes down from higher elevations, using its wings to slow its descent.
- Breeding and Lekking: Kākāpō have a unique mating system called lekking, where males gather at specific areas and emit loud, low-frequency "booming" calls to attract females. These booms can carry for several kilometers. The species is also notable for its infrequent breeding, tied to the mast fruiting of native trees like the rimu, which occurs every few years.
- Solitary: They are generally solitary and only come together during the breeding season.
- Conservation Status
- Critically Endangered: The kākāpō once flourished throughout New Zealand, but with the arrival of humans and introduced predators like rats, stoats, and cats, their population dwindled dramatically. By the late 20th century, only about 50 birds remained.
- Conservation Efforts: Today, thanks to intensive conservation programs, the population has slowly grown to around 250 individuals. The birds are now housed on predator-free offshore islands such as Codfish Island and Anchor Island, where they are closely monitored by conservationists.
- Hand-Raising and Monitoring: Conservationists have implemented strategies like hand-raising chicks, monitoring individual birds with radio transmitters, and managing breeding cycles.
- Evolutionary Background
- Origins: The kākāpō is a member of the Strigopidae family, which includes other New Zealand parrots like the kea and the kākā. The ancestors of these parrots are believed to have arrived in New Zealand from Gondwana over 60 million years ago, long before New Zealand split from the ancient supercontinent.
- Isolation: Due to New Zealand’s geographic isolation and lack of mammalian predators before human settlement, the kākāpō evolved without the need for flight. This environment allowed it to adapt to ground-dwelling behaviors and become a highly specialized, nocturnal herbivore.
- Flightless Adaptation: Over time, flight became unnecessary, and the bird developed robust legs for walking and climbing. Its large body size and wings that are adapted for balance and gliding, rather than flight, are consistent with its long-term evolution in a predator-free environment.
- Loss of Defenses: One of the consequences of evolving in an environment without mammalian predators was the loss of defense mechanisms against such animals. This made the kākāpō highly vulnerable when rats, stoats, and other mammals were introduced by Polynesians and Europeans.
- Cultural Significance
- Māori Connection: The kākāpō has deep cultural significance to the Māori people, who traditionally hunted the bird for its meat and feathers. The feathers were used in clothing, and kākāpō bones were made into tools. However, traditional Māori hunting practices did not lead to the bird’s extinction; rather, it was the introduction of foreign predators and habitat destruction that drove the species toward the brink.
- Challenges to Survival
- Low Reproductive Rate: The kākāpō's reproductive cycle is slow and closely tied to the irregular fruiting of certain trees. This makes population recovery a slow process.
- Genetic Bottleneck: With such a small population, genetic diversity is a concern. Conservationists have been using genetic techniques to carefully manage breeding to avoid inbreeding and increase the health of the population.
- Predator-Free Islands: The kākāpō recovery relies heavily on maintaining predator-free environments. Vigilant control of invasive species is necessary to ensure the bird’s continued survival.
- Conservation Success
Despite being on the verge of extinction, the kākāpō conservation program is considered one of the great success stories of wildlife conservation. Advances in understanding their unique biology, habitat needs, and threats have helped conservationists significantly increase the population from its nadir in the 1990s.
The kākāpō is not just a symbol of the unique evolutionary path taken by New Zealand's wildlife but also a powerful emblem of the fight against extinction. While the species' future remains uncertain, ongoing conservation efforts give hope for the continued recovery of this remarkable parrot.
Tell me about the two colour forms, olive and green, and what advantage(s) there are in having two color forms.
The kākāpō has two main color forms: olive and green, both of which serve as natural camouflage. These colors blend remarkably well with the mossy, forested environments where the kākāpō lives. Here’s more about the two forms and the potential advantages of having different color morphs:
- Olive and Green Forms
- Olive Form: Kākāpōs with this form display a combination of olive-brown and yellow-green feathers, with streaks of brown and black. This color variation helps them blend into the underbrush and mossy environments, especially in low-light conditions, as the olive tones mirror the hues of dried leaves and bark.
- Green Form: This form is a brighter green, closer to the vibrant shades of native forest foliage. These kākāpōs have predominantly green feathers with darker specks, resembling the green leaves and ferns of their habitat.
Both color forms exhibit mottled patterns, further enhancing their ability to avoid detection by predators, especially in dense vegetation.
- Advantages of Two Color Forms
Having multiple color forms provides the kākāpō with some potential evolutionary advantages:
- Enhanced Camouflage in Varied Environments
- Seasonal and Habitat Variability: New Zealand’s forests can vary in color and texture depending on the season, local vegetation, and specific environments. The olive form might provide better camouflage in areas with more dried foliage, bark, or during certain seasons, while the green form may be better suited to environments with denser green vegetation. By having both color forms within the population, kākāpōs increase their chances of avoiding detection across different terrains and seasonal changes in the environment.
- Low Light and Night Activity: Since kākāpōs are nocturnal and inhabit dense, shaded forests, their camouflage needs to be effective in low-light conditions. Both color forms likely offer benefits depending on the specific forest conditions, as well as the angle and intensity of light at different times of night.
- Predator Evasion
- Diversified Defense: Historically, New Zealand lacked mammalian predators, so the kākāpō’s camouflage evolved primarily to evade aerial predators like the now-extinct Haast’s eagle and other large birds of prey. Having two different color forms could have helped reduce the likelihood of detection from these predators, as the slight differences in appearance may have confused or misled attackers hunting by sight.
- Post-Predator Introduction: With the arrival of humans and mammalian predators (stoats, rats, cats), color variation could still offer some benefit in evading detection from ground-based predators, though kākāpōs’ lack of other defensive behaviors made them highly vulnerable.
- Genetic Diversity and Evolutionary Resilience
- Genetic Variation: Color polymorphism within a population often reflects underlying genetic diversity, which can be beneficial for the species as a whole. Maintaining genetic variation through different color morphs may contribute to overall fitness, particularly in changing environments.
- Selection Pressures: Having two distinct color forms might also help the population respond more flexibly to shifts in environmental pressures, such as habitat changes or the presence of predators. If one color form provides better camouflage under certain conditions, individuals of that form might have a slight survival advantage, leading to a natural balancing of the population based on environmental shifts.
- Lack of Strong Predation Pressures
Interestingly, since the kākāpō evolved in a land with virtually no mammalian predators, the significance of these color forms was probably more subtle compared to species in predator-dense regions. The variations in olive and green forms likely enhanced general camouflage but did not need to develop into extreme distinctions, as their main threat came from the air.
While modern-day conservation focuses on maintaining kākāpō populations, including their genetic diversity, the two color forms remain a vestige of the bird's evolutionary past, offering both camouflage benefits and a glimpse into the adaptability of this unique species.
In this context, what is Negative Frequency-Dependent Selection (NFDS)?
Negative frequency-dependent selection is a type of natural selection where the fitness (survival and reproductive success) of a particular phenotype increases when it is rare in the population, and decreases when it becomes more common. In simpler terms, individuals with less common traits tend to have a selective advantage because their rarity provides a benefit, often by avoiding certain threats or competition. This mechanism helps maintain genetic diversity within a population.
In the context of the kākāpō’s two color forms (olive and green), negative frequency-dependent selection could help explain why both color forms persist in the population. Here’s how it works:Example:
- Camouflage and Predator Evasion
- If one color form (say, green) becomes more common, predators might become better at spotting and hunting individuals with that coloration because they are more familiar with that pattern.
- Individuals with the rarer olive form, however, might be less easily detected by predators, as their less common appearance could be less recognizable or expected in the environment.
- As a result, individuals with the rarer color form might survive better and reproduce more successfully, leading to a balancing of the frequency of the two color forms in the population over time.
- Balancing Genetic Diversity
- Negative frequency-dependent selection helps maintain genetic diversity in a population by preventing any one color form (or trait) from becoming too dominant. If the olive form were to become too common, the same principle could apply in reverse, giving a survival advantage to individuals with the green form when it becomes rare.
- Avoiding "Search Image" Predation
- Some predators develop a "search image" for common prey characteristics, which makes them more efficient at hunting prey that looks a certain way. If a predator becomes good at detecting the more common color form of the kākāpō, individuals with the rarer form might have an advantage because they don't match the predator’s search image.
In the kākāpō, if the environment changes seasonally or spatially, or if predators were more successful at spotting one color form over another, negative frequency-dependent selection could ensure that neither the olive nor the green form becomes overwhelmingly dominant. This selective pressure maintains a balance between the two morphs, which helps the species as a whole by preserving color diversity that aids in camouflage and survival in different environments.
In short, negative frequency-dependent selection in the kākāpō could help explain why both the olive and green forms persist in the population, as their rarity can provide a survival advantage, keeping both color morphs in balance.
They have just published their findings, open access, in the journal PLOS Biology.
According to information from PLOS, published in ScienceDaily:
Flightless parrot in New Zealand developed different feather colors to evade predatory birds
Genome sequencing shows olive feather coloration evolved around the same time as two now-extinct predators
Aotearoa New Zealand's flightless parrot, the kākāpō, evolved two different color types to potentially help them avoid detection by a now-extinct apex predator, Lara Urban at Helmholtz AI, Germany and colleagues from the Aotearoa New Zealand Department of Conservation and the Māori iwi Ngāi Tahu, report in the open-access journal PLOS Biology, publishing September 10.
The kākāpō (Strigops habroptilus) is a nocturnal, flightless parrot endemic to New Zealand.
It experienced severe population declines after European settlers introduced new predators.
By 1995 there were just 51 individuals left, but intense conservation efforts have helped the species rebound to around 250 birds.
Kākāpō come in one of two colors -- green or olive -- which occur in roughly equal proportions.
To understand how this color variation evolved and why it was maintained despite population declines, researchers analyzed genome sequence data for 168 individuals, representing nearly all living kākāpō at the time of sequencing.
They identified two genetic variants that together explain color variation across all the kākāpō they studied.
Scanning electron microscopy showed that green and olive feathers reflect slightly different wavelengths of light because of differences in their microscopic structure.
The researchers estimate that olive coloration first appeared around 1.93 million years ago, coinciding with the evolution of two predatory birds: Haast's eagle and Eyles' harrier.
Computer simulations suggest that whichever color was rarer would have been less likely to be detected by predators, explaining why both colors persisted in the kākāpō population over time.
The results suggest that kākāpō coloration evolved due to pressure from apex predators that hunted by sight.
This variation has remained even after the predators went extinct, around 600 years ago.
The authors argue that understanding the origins of kākāpō coloration might have relevance to the conservation of this critically endangered species.
They show that without intervention, kākāpō color variation could be lost within just 30 generations, but it would be unlikely to negatively impact the species today.
By using a comprehensive genomic library for the species, we have explained how the current colour morphs of kākāpō might be a result of pressure from extinct predators. Using genomics to understand the current significance of such characteristics is important as we seek to restore the mauri (life force) of kākāpō by reducing intensive management and returning them to their former habitats.
Andrew Digby, co-author
Kākāpō Recovery Programme
Department of Conservation
Invercargill, Murihiku, Aotearoa New Zealand.
AbstractAs the design of a super-intelligent, omniscient designer, two colour forms of the same species, neither of which is advantageous compared to the other, makes no sense at all. It merely wastes resources and introduces more complexity than is necessary - a hallmark of unintelligent, mindless design, but the antithesis of good, intelligent design.
The information contained in population genomic data can tell us much about the past ecology and evolution of species. We leveraged detailed phenotypic and genomic data of nearly all living kākāpō to understand the evolution of its feather color polymorphism. The kākāpō is an endangered and culturally significant parrot endemic to Aotearoa New Zealand, and the green and olive feather colorations are present at similar frequencies in the population. The presence of such a neatly balanced color polymorphism is remarkable because the entire population currently numbers less than 250 birds, which means it has been exposed to severe genetic drift. We dissected the color phenotype, demonstrating that the two colors differ in their light reflectance patterns due to differential feather structure. We used quantitative genomics methods to identify two genetic variants whose epistatic interaction can fully explain the species’ color phenotype. Our genomic forward simulations show that balancing selection might have been pivotal to establish the polymorphism in the ancestrally large population, and to maintain it during population declines that involved a severe bottleneck. We hypothesize that an extinct apex predator was the likely agent of balancing selection, making the color polymorphism in the kākāpō a “ghost of selection past.”
Introduction
About a century ago, population geneticists began to study the evolution of polymorphisms at genetic loci [1]. We have now reached a milestone where we can examine nucleotide variation across the entire genome of every single individual of a species. This remarkable feat has been accomplished for the kākāpō (Strigops habroptilus) [2], a critically endangered flightless parrot species endemic to Aotearoa New Zealand that is considered a taonga (treasure) of Ngāi Tahu, a Māori iwi (tribe) of Te Wai Pounamu (the South Island of Aotearoa) [3–5]. The genomic data that has been generated for this species now enables us to study population genomics at an unprecedented resolution, improving our understanding of the evolutionary forces impacting this threatened species with the potential to inform their conservation and recovery in partnership with Ngāi Tahu [2,4,6,7].
In this study, we explore the puzzling phenomenon of the kākāpō feather color polymorphism (“green” and “olive” phenotypes) and how this severely bottlenecked species managed to retain its phenotypic diversity. The kākāpō has experienced a population decline and significant genetic drift over the past 30,000 years (30 KYA), followed by a sharp, anthropogenically induced population bottleneck resulting in just 51 surviving individuals in 1995 [7]. Under the close management of the Aotearoa New Zealand Department of Conservation Te Papa Atawhai Kākāpō Recovery Programme in partnership with Ngāi Tahu [4,8], the population size has increased to 247 birds located on several predator-free islands [as of August 1, 2024]. Despite these severe bottleneck events, the population exhibits a relatively balanced distribution of green and olive individuals; to understand the evolution of this color polymorphism, we here assess the phenotype’s genomic basis and how the genetic polymorphism was first established and has since been maintained in the population.
Population genetic theory hereby stipulates that newly emerged genetic variants (i.e., mutations) are rarely expected to reach appreciable allele frequencies when they evolve neutrally since they often get lost through genetic drift [9]. Kimura’s neutral theory of molecular evolution suggests that most genetic polymorphisms are neutral (or slightly deleterious) because if a mutation conferred a selective advantage, it would be expected to rise to fixation, replacing the ancestral allele [10]—unless the frequency rise of such beneficial variants is halted by one or more counteracting evolutionary forces. Balancing selection can theoretically balance allele frequencies and produce stable genetic polymorphisms, for example, through negative frequency-dependent selection (NFDS), overdominance, antagonistic selection, or temporally and spatially varying selection [11]. To understand the establishment and maintenance of genetic polymorphisms, we therefore need to first reject the null hypothesis of neutral evolution, and then describe the evolutionary forces that help maintain the genetic polymorphism [11–13]. In the case of the kākāpō’s genetic polymorphism that underlies its color polymorphism, we therefore have to assess how the genetic polymorphism was not randomly lost in the species’ large ancestral population, and how it has since been maintained despite population decline and a severe population bottleneck.
Understanding the establishment and maintenance of the kākāpō polymorphism might be of importance for ongoing conservation efforts since the significant majority (nearly 70%) of the wild founder population from 1995 were of green color. Whether the color polymorphism is likely to impact fitness in the absence of current intensive conservation management is therefore of potential conservation relevance—especially given the long-term plans of the Kākāpō Recovery Programme and Ngāi Tahu to restore this critically endangered species beyond predator-free islands. Why the kākāpō species has maintained the green and olive phenotype has so far remained elusive. Before the arrival of tūpuna Māori in AD 1280 [14], the only predators of the kākāpō were avian [15], the vast majority of which hunt by sight. While the apex predators, the Haast’s eagle (Hieraaetus moorei) and the Eyles’ harrier (Circus teauteensis), went extinct approximately 600 years ago [14], we hypothesize that the kākāpō color polymorphism could be a consequence of selective pressures through this past predation. For example, NFDS through search image formation in the avian predators can theoretically maintain such polymorphisms [16].
To explore which hypothesis best explains the kākāpō color polymorphism, we created and analyzed detailed phenotypic data of kākāpō plumage together with high-coverage genomic data of nearly the entire kākāpō species (n = 169; as of January 1, 2018) [2,11]. We found that two epistatically interacting single-nucleotide polymorphisms (SNPs) at the end of chromosome 8 can explain the color polymorphism of all individuals. A candidate gene analysis in this genomic region allowed us to hypothesize a structural color polymorphism, which we explored with subsequent optical analyses. The nucleotide divergence between the two indicator haplotypes predicted that the color polymorphism evolved circa 1.93 MYA, around the time when the avian kākāpō predators evolved. Using genomic forward simulations, we determined that the polymorphism’s establishment is highly unlikely under neutral evolution, while any selective advantage of the novel color morphology would have likely led to its rapid fixation. We show that the effects of balancing selection would have been sufficient to establish the polymorphism in the large ancestral population. Our simulations show that the polymorphism could have subsequently been maintained despite declining population size and a severe kākāpō population bottleneck. Also this polymorphism has been maintained despite dramatic ecological changes in Aotearoa New Zealand approximately 600 years ago when several indigenous bird species including the major natural kākāpō predator species became extinct [14]. Based on this evidence, we propose that now-extinct apex predators were the likely agent of balancing selection, which would make the color polymorphism in the kākāpō a “ghost of selection past.”
[hellip;]
Fig 1. The kākāpō feather color polymorphism.
(A) Green (left) and olive (right) kākāpō individuals; the photographs show the kākāpō individuals Uri (left) and Bravo (right) who are full siblings. The inserts show the standardized photography that was applied for color assessment across the extant kākāpō population (Material and Methods). (B) Manhattan plot of the mixed-model GWAS between all bi-allelic SNPs and the binary color polymorphism phenotype (Material and Methods); the horizontal line indicates the genome-wide significance line after Bonferroni multiple testing correction. The genome-wide significant hit at the end of chromosome 9 represents a single SNP, which we therefore discarded as noise. Inlet: Zoom-in of the Manhattan plot on the end of chromosome 8 (from 6.25 × 107 bp to the end of the chromosome); the two most significant SNPs Chr8_63055688 and Chr8_63098195 are highlighted in orange color. All photographs are originals taken by the authors of this manuscript. The code to generate this figure can be found in https://zenodo.org/records/13302801. For data see the “Data and code availability” section. GWAS, genome-wide association study; SNP, single-nucleotide polymorphism.
https://doi.org/10.1371/journal.pbio.3002755.g001
Fig 2. Optical analyses of kākāpō feathers of both color polymorphisms.
(A) SEM images of 3 green (left 3 columns) and 3 olive (right 3 columns) feather barbules at different resolutions (rows); the green feathers show a smoother surface than the olive ones. (B) Photoreflectometry of near-infrared/visible wavelengths in the feather tips; the relative reflectance of an exemplary olive and green is plotted over the wavelength of the reflected light (Material and Methods). All photographs are originals taken by the authors of this manuscript. The data underlying this figure can be found in https://zenodo.org/records/13302801. SEM, scanning electron microscopy.
Discussion
By combining deep genomic and detailed phenotypic data with computer simulations and optical analyses, we have studied the origin and evolution of the kākāpō feather color polymorphism. We describe the putative genomic architecture of this phenotype and establish that a dominance epistatic interaction of 2 biallelic single-nucleotide genetic variants can explain the phenotype of all 168 birds, which had paired genomic and phenotypic data. Integrating this genomic architecture with genomic forward simulations, we explain the likely evolution and puzzling maintenance of this balanced polymorphism in the heavily bottlenecked kākāpō population.
Established genetic polymorphisms are rare and challenging to identify due to the need to rule out neutral evolution and determine the evolutionary forces maintaining them, such as balancing selection [11]. Rejecting neutral evolution requires assessing the genetic basis, fitness consequences, and potential selective agents of the phenotype. If directly measuring fitness effects is not feasible, balancing selection can still be inferred by rejecting neutral evolution and positive selection as explanations. Here, we estimated that the kākāpō feather color polymorphism was roughly established around 1.93 million years ago as an oligogenic trait, with green as the likely ancestral phenotype. Through genomic simulations, we found that neutral and positive evolution were highly unlikely, suggesting balancing selection through NFDS as a possible driver in establishing this polymorphism …
Urban L, Santure AW, Uddstrom L, Digby A, Vercoe D, Eason D, et al. (2024)
The genetic basis of the kākāpō structural color polymorphism suggests balancing selection by an extinct apex predator.
PLoS Biol 22(9): e3002755. https://doi.org/10.1371/journal.pbio.3002755
Copyright: © 2024 The authors.
Published by PLoS. Open access.
Reprinted under a Creative Commons Attribution 4.0 International license (CC BY 4.0)
As the result of evolutionary dynamics involving arms races between a species and two competitors it makes perfect sense and explains why one colour form never progressed to fixation in the population. If a camouflage strategies worked against one predator then the other predator gained an advantage by being able to detect it, so the other form would tend to increase, any tendency for one to become predominant would have increased the selection pressure against it and favoured the other, so an evolutionary dynamic was reached in which both colour forms are present in about equal proportions.
Now the apex predators are both extinct there are no environmental selectors which change that balance, so we have the two colour forms which, in today's New Zealand environment are inexplicable except in terms of that evolutionary dynamic with two competing apex predators.
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