The (un)reasonable beauty: What factors shaped the evolution of Paradisaeidae?


Source: https://ed.everwideningcircles.com/birds-of-paradise/

Abstract

Birds of paradise are a diversified family characterised by truly paradisical morphology and intricate behaviour. Evidence for the role of habitat, sexual selection (lek mating) and genes in creating well-known extravagant phenotypes, puzzling beheaviours and the presence of a multitude of species are present yet it is difficult to choose one perfect and complete theory for the evolution of birds of paradise.

Introduction

Avian family ​​Paradisaeidae, commonly known as birds of paradise, is composed of 42 species in 15 genera[1] that inhabit varied terrains ranging from humid undercoats of rainforest to gentle slopes of New Guinea, islands surrounding it and northwestern Australia [2, 3, 4,5].
High latitudes, where habitats of birds of paradise are located, are characterised by great biodiversity[6]. Yet ​​​​Paradisaeidae amaze with the multitude of species that represent it and the immensity of their morphology and behaviour.
Phylogenetic studies have distinguished the 41 species as a result of analysis of mitochondrial and nuclear genes[2,5]. Studies have shown that the family evolved from a common crow-like ancestor who lived 24 million years ago (late Oligocene/ early Miocene)[2,5,7]. Until present day some species, such as Lycocorax pyrrhopterus, have crow-like phenotypes, display poor sexual dimorphism and simple mating rituals[2,5,7].
What became the identification mark of this family are the extravagant looks and behaviours of males. That the vast majority of them exhibit decorative elements such as vividly-coloured plumage or magnificent tail shapes in addition to performing intricate dance routines in order to attract the female. The above greatly varies between species in males, while females in most cases remain alike between species, being gray, brown or beige and lacking in decorative elements.
This article serves the purpose of summarising the current state of knowledge on evolution of ​​Paradisaeidae and evaluating the impact of environment, sexual selection and genes on it.
Figure 1. Phylogeny of ​​Paradisaeidae proposed by Irestedt et al. in ‘An unexpectedly long history of sexual selection in birds-of-paradise’. The five main clades of birds of paradise can be seen (A-E).
Source: Irestedt, Martin et al. ‘An unexpectedly long history of sexual selection in birds-of-paradise’

Methodology

Articles were searched for using Google Scholar search engine and ResearchGate. When describing behaviours, the Author used ‘The 39 species’ by Cornell Lab of Ornithology on YouTube (https://www.youtube.com/watch?v=KkMwZgtHVnI) as a reference helpful in determining to which species an individual seen on cited videos belongs to if the sources do not provide such information.

Evolution of colour

Prost et al. found 213 genes to be under selection in eight species of birds of paradise. These genes were associated with synthesis and transport of melanin, a pigment which gives feathers dark colour. One of them, ADAMTS20 is responsible for the development of melanocytes which are responsible for plumage patterns in different families of birds therefore this gene is highly likely to be related to evolution of feather ornaments in birds of paradise as well[8].
Lek mating system leads to the primacy of vivid feather colour over dull colour in the evolution. It was observed that the development of carotenoid (yellow, red, orange) pigment in the feathers was accelerated and hence the carotenoid-melanin ratio increased with every generation[5]. At the same time, sexual selection corelates negatively with bright colours in female plumage[8, 9].
Although they are famous for the magnificent colours of their plumage, birds of paradise usually have black feathers as well (figure 3, 4, 5). They tend to line the bright areas. McCoy and Prum discovered that in Parotia wahnesi feathers are able to absorb up to 99.5% of light as they have special structures called barbules. They suggested that the development of two colour extremities in plumage is to promote enhancement of the more crucial, light, colours by black[10,11].
Figure 2. The illusion of differently-coloured Lewe’s Parotia feathers from different perspectives a) fronto-parallel view b) oblique view. Source: ‘Dramatic color changes in a bird of paradise caused by uniquely structured breast feather barbules’ by Stavenga, D. et al. (edited).
Intricate feather structure can also be observed in Lawes\’s Parotia (Parotia lawesii) which modifies the perception of its feathers when they are subjected to light from different angles[8, 12] (figure 2).
Three genes associated with eye development and anatomy are thought to co-evolve with coloration[8]. On the other hand, the link between eye development and coloration is uncertain because good vision is crucial for nutrition of birds of paradise and colour differencing can be used for multiple purposes related to mating such as adorning the ground with red berries performed by Western parotia.

Diversity and speciation

Many bird of paradise species such as the Lesser Bird of Paradise (Paradisaea minor) display lek mating behaviours. Lekking is a behaviour observed in birds, insects and mammals where two or more males perform courtship displays for the observing female. This behaviour increases competition within the species, where a strong phenotype is presumably necessary to succeed. Irestedt et al. found that old genera such as Paradisaea or Parotia, all species of which display lekking behaviours, are morphologically alike between different species of one genre[6]. This would imply that lekking does not profoundly enhance morphological diversity within a genre. Furthermore, speciation rates of Paradisaea and Parotia which were calculated by Irestedt et al. are mediocre[6]. To summarise, their research suggests that sexual selection and competition between males does not significantly influence speciation and morphological diversifity of birds of paradise. Hence reasons for fast and abundant in non-practical traits evolution must be sought for elsewhere.
Contrary to that, previous research of Christidis and Schodde, suggested that diversification of species was accelerated by sexual selection[13]. They also promote views of other scientists, Ten Cate and Bateson (1957), who proposed that birds of paradise prefer partners of novel morphology in order to prevent mating of distinct but related species (interbreeding)[13]. But this mechanism is either rare or uneffective as previously cited and more modern studies prove that interbreeding is common in ​​Paradisaeidae and species such as Elliot’s bird of paradise (figure 3) are believed to be results of it[14].
Figure 3. Eliott’s bird of paradise. A species believed to be a hybrid of Black Sicklebill and Arfak Astrapia.[15]
Source: https://www.wikidata.org/wiki/Q5365449 (Accessed 23.12.2021)
Prost and associates found that bursts of transposable elements (TEs) activity positively correlate with speciation of birds of paradise. Transposable elements or ‘jumping genes’ can shift their location in the genome[16, 17, 18]. They are abundant in the genomes of animals, fungi and especially plants, in which they constitute up to 80% of nuclear DNA[17]. Described TEs have different functions among which the most common are mediating in genome recombination or increasing rates of gene rearrangement[17, 18].
Sex of birds of paradise is determined by two sex chromosomes called W anz Z. ZW genotype signifying a female individual and ZZ a male one[19]. These chromosomes were found to evolve rapidly[19]. Especially, the Z chromosome exhibits higher evolutionary rates compared to autosomes. The Z chromosomes were found to be highly prone to mutation, for example they exhibit a higher rate of inverse mutations (which cracks the chromosome and inverts the unbound piece by 180 degrees) resulting in profound changes. This is because they are more often transmitted in males[19].

Role of habitat and behaviour

Birds of paradise is a family of species endemic to subtropical areas of the southern hemisphere. The majority of species inhabit New Guinea with some residing in the Molucca islands and north-eastern Australia[4, 20].
Habitat might play a role in the richness of courtship displays. It was observed that birds which inhabit the undercoat of rainforest tend to display a dance sequence more abundant in gestures than their counterparts living in tree canopies[5]. Naturally, densely deployed trees block the sunlight forcing members of ​​Paradisaeidae inhabiting the undercoat to live in the shadow. Their response is creating more explicit dance sequences in order to compensate for lack of light and worsened vision which is a result of this deficiency.
Said dances are composed of countless stances, gestures and steps: the Vogelkop superb bird of paradise is a prime example. This bird can famously (and amusingly) alter its shape into nearly oval, displaying lazure feathers which resemble a smiley face (figure 4, 5). The majority of birds of paradise can produce intricate sounds that compose songs to accompany courtship displays as well.
Some species go further than producing a dance routine- Western parotia (Parotia sefilata) prepares the ground on which it is to perform as well. The preparations include picking and throwing away fallen leaves and decorating the floor with red berries, presumably to attract the female[21]. Furthermore, P. sefilata can rub shed snake skin against branches: scientists have not presented one view on why this behaviour occurs. Some believe it is to use the skin as a cleaning cloth to complete the tidying sequence while some believe it is to transfer the scent of the snake onto the branch the female is expected to sit on[21].

Figure 4. The Vogelkop superb bird of paradise amidst its song.
Source: https://economictimes.indiatimes.com/magazines/panache/all-about-vogelkop-superb-bird-of-paradise-the-new-species-in-the-avian-world/articleshow/63856825.cms

Figure 5. The Vogelkop superb bird of paradise, performing.
Source: https://myonebeautifulthing.com/2015/04/28/birds-of-paradise-by-the-dashboard-light/

Footnotes

[1] Winkler, David W et al. Birds of the World- The Cornell Lab of Ornithology. Https://brandsoftheworld.org/bow/species/paradi 7/1.0/introduction
Accessed 16.12.2021
[2] Prost, Stefan et al. ‘Comparative Genomics and Genome Evolution in birds-of-paradise’
March 2018.
DOI: 10.1101/287086
[3]- ‘Birds of paradise’. National Geographic. nationalgeographic.com
Accessed 30.11.2021
[4] ‘Crows, mudnesters, melampittas, Ifrit, birds-of-paradise’ IOC World Bird List v11.2. worldbirdnames.org. Accessed 30.11.2021
[5] Marley, Sarah. ‘Evolution of dance and colour in the birds of paradise’. Animal Ecology in Focus- British Ecological Society. animalecologyinfocus.com 11.04.2018. Accessed 30.11.2021
[6] Irestedt, Martin et al. ‘An unexpectedly long history of sexual selection in birds-of-paradise’. BMC Evolutionary Biology 9(1):235.
DOI:10.1186/1471-2148-9-235
[7] Dowle, Eddy J, Morgan-Richards, Mary, and Trewick, Steven A. ‘Molecular evolution and the latitudinal biodiversity gradient’. Nature Heredity 110 (2013): 501-510
DOI: 10.1038/hdy.2013.4
[8] Prost, Stefan et al. ‘Comparative analyses identify genomic features potentially involved in the evolution of birds-of-paradise’. GigaScience, 8(5) 2019.
DOI: 10.1093/gigascience/giz003
[9] Dale, James et al. ‘The effects of life history and sexual selection on male and female plumage colouration’. Nature 527: 367-370 2015.
DOI: 10.1038/nature15509
[10] Perkins, Sid. ‘Back to Black: How Birds-of-Paradise Get Their Midnight Feathers’. Scientific American. Accessed December 2021.
https://www.scientificamerican.com/article/back-to-black-how-birds-of-paradise-get-their-midnight-feathers/
[11] McCoy, Dakota E and Prum, Richard O, ‘Convergent evolution of super black plumage near bright color in 15 bird families’. Journal of Experimental Biology 222(18) 2019.
DOI: 10.1242/jeb.208140
[12] Stavenga, Doekele et al. ‘Dramatic color changes in a bird of paradise caused by uniquely structured breast feather barbules’. Proceedings of the Royal Society B: Biological Sciences 278(1715):2098-104.
DOI: 10.1098/rspb.2010.2293
[13] Christidis, Les and Schodde, Richard. ‘Sexual selection for novel partners: A mechanism for accelerated morphological evolution in the birds-of-paradise (Paradisaeidae)’. Bulletin of the British Ornithologists\’ Club 113:169-172 1993.
[14] Google Arts & Culture. ‘Elliot’s Bird of Paradise’. Accessed 21.12.2021 https://artsandculture.google.com/entity/elliot-s-bird-of-paradise/m06w78d3
[15] ‘Elliot’s Bird of Paradise’. Beauty of Birds. Accessed 27.12.2021.
https://www.beautyofbirds.com/elliotsbirdofparadise.html
[16] Pray, Leslie. ‘Transposons, or Jumping Genes: Not Junk DNA?’. Nature Education 1(1):32 2002. https://www.nature.com/scitable/topicpage/transposons-or-jumping-genes-not-junk-dna-1211/
[17] Serrato-Capuchina, Antonio and Matute, Daniel R. ‘The Role of Transposable Elements in Speciation’ Genes 9(5):254.
DOI: 10.3390/genes9050254
[18] Ricci, Marco et al. ‘Transposable Elements Activity is Positively Related to Rate of Speciation in Mammals’. Journal of Molecular Evolution 86:303–310 2018.
DOI: doi.org/10.1007/s00239-018-9847-7
[19] Xu, Luohao et al. ‘Dynamic evolutionary history and gene content of sex chromosomes across diverse songbirds’ October 2018.
DOI: 10.1101/454843
[20] Heads, Michael. ‘Birds of paradise, vicariance biogeography and terrane tectonics in New Guinea’ Journal of Biogeography 29(2): 261-283 2002.
DOI: 10.1046/j.1365-2699.2002.00667.x
[21] ‘Bird Of Paradise: Appearances COUNT! | Animal Attraction | BBC Earth’. 30.12.2015 YouTube video. Posted by ‘BBC Earth’. Accessed December 2021.
https://www.youtube.com/watch?v=iTmHtxJpEWE

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