Feather Evolution from Precocial to Altricial Birds (2024)

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Zool Stud
v.58; 2019
PMC6917565

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Zool Stud. 2019; 58: e24.

Published online 2019 Sep 16. doi:10.6620/ZS.2019.58-24

PMCID: PMC6917565

PMID: 31966325

Chih-Kuan Chen,^1,^2,^* Hao-Fen Chuang,³ Siao-Man Wu,⁴ and Wen-Hsiung Li^2,^5,^6,^*

Author information Article notes Copyright and License information PMC Disclaimer

Abstract

Birds are the most abundant terrestrial vertebrates and their diversity is greatly shapedby the feathers. How avian evolution is linked to feather evolution has long been afascinating question. Numerous excellent studies have shed light on this complexrelationship by investigating feather diversity and its underlying molecular mechanisms.However, most have focused on adult domestic birds, and the contribution of featherdiversity to environmental adaptation has not been well-studied. In this review, wedescribed bird diversity using the traditional concept of the altricial-precocial spectrumin bird hatchlings. We combined the spectrum with a recently published avian phylogeny toprofile the spectrum evolution. We then focused on the discrete diagnostic character ofthe spectrum, the natal down, and propose a hypothesis for the precocial-to-altricialevolution. For the underlying molecular mechanisms in feather diversity and birdevolution, we reviewed the literature and constructed the known mechanisms for feathertract definition and natal down development. Finally, we suggested some future directionsfor research on altricial-precocial divergence, which may expand our understanding of therelationship between natal down diversity and bird evolution.

INTRODUCTION

Avian specialty and the precocial-altricial spectrum

Birds, with more than 10,000 known species, are the most abundant terrestrialvertebrates. They are highly diverse in body size, shape, and color (Wright 2006). Birdevolutionary innovations include feathers, toothless beaked jaws, hard-shelled eggs, ahigher metabolic rate, and a light but strong skeleton, enabling them to occupy differentecological niches. Thus, birds are an excellent model to study animal evolution andenvironmental adaptations.

The feathers show the highest degree of complexity and diversity among the evolutionarynovelties in birds (Chen et al. 2015, Prum 2005, Prum and Brush 2002, Strasser et al.2015). For example, down feathers composed of barbs and barbules can keep the body warm,while contour feathers possessing rachis provide physical protection and attraction.Feather diversity has likely contributed to avian diversity.

Avian hatchlings display variation in apparent maturity, which is called thealtricial-precocial spectrum (Table 1). The hatchlings of altricial birds, such asPsittaciformes and Passeriformes songbirds, are close to the embryonic state, with almostnaked skin and closed eyes. On the other hand, precocial hatchlings, such as Galliformesand Anseriformes, are close to the adult state, with open eyes and feathers (Starck andRicklefs 1998). The functional maturity of the hatchlings determines the care they needfrom their parents and the environment to which they are going to adapt (Starck andRicklefs 1998, Vleck and Vleck 1987).

Table 1. Diagnostic features of developmental modes in birdhatchlings

Developmental modea	Plumage	Eyes	Nest attendance	Parental care
P1	Contour feather	Open	Leave	None
P2	Down	Open	Leave	Brooding
P3	Down	Open	Leave	Food showing
P4	Down	Open	Leave	Parental feeding
SemiP	Down	Open	Nest area	Parental feeding
SemiA1	Down	Open	Stay	Parental feeding
SemiA2	Down	Closed	Stay	Parental feeding
A	None	Closed	Stay	Parental feeding

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^aP1: precocial 1; P2: precocial 2; P3: precocial 3; P4: precocial 4;SemiP: semiprecocial; SemiA1: semialtricial 1; SemiA2: semialtricial 2; A:altricial.

Plumage is a main diagnostic feature in defining the altricial-precocial spectrum.However, the definition is not clear-cut, and the underlying molecular mechanism is notwell characterized. In this review, we first re-analyzed the evolutionary pattern of thealtricial- precocial spectrum using a recently published avian phylogeny. Second, we thensurveyed the literature and hypothesized a scenario for the evolution feathers. Third, wereviewed the known molecular mechanisms responsible for the natal down divergence anddiscussed unresolved questions. Finally, we suggested possible research directions touncover the mystery of feather evolution in modern birds.

Definitions of precocial and altricial birds and their evolution

Altricial and precocial hatchling divergence has been thought to be associated withenvironmental adaptation. However, how to define the divergence is still debated (Starckand Ricklefs 1998). In habitat selection, most altricial birds tend to nest above ground,and their chicks need to spend more time growing before they can leave the nest on theirown (Bicudo 2010). In contrast, most precocial birds tend to be ground nesting, and theirchicks can walk away from the nest soon after hatching. Several morphological andbehavioral characters in hatchlings have been used as diagnostic features for the spectrum(Table 1), such as downy plumage, motor activity, locomotor activity, parental care, foodsearch and feed alone, staying in the nest, eyes closed at hatching, without externalfeathers at hatching, no interaction with parents, and contour feathers in hatchlings(Bicudo 2010, Nice 1962, Skutch 1976, Starck and Ricklefs 1998). A comprehensive analysisreorganizing and summarizing the spectrum is shown in table 1 (Starck and Ricklefs 1998).

We then plotted the updated altricial-precocial spectrum to a recently published avianphylogeny that covers by far the most bird families (Fig. 1) (Hart et al. 2017, Prum etal. 2015, Starck and Ricklefs 1998). Due to limited data availability, we only mapped theavian species to four modes: precocial, semiprecocial, semialtricial, and altricial modes.Several patterns consistent with previous findings were revealed. First, the trend fromprecocial toward altricial avian evolution is supported by studies in both fossils andextant birds (Charvet and Striedter 2011, Starck and Ricklefs 1998, Xing et al. 2017, Zhouand Zhang 2004). The same trend is also seen in the phylogeny (Fig. 1). Second, theprecocial toward altricial evolution occurred multiple times (Charvet and Striedter 2011,Chen et al. 2016, Starck and Ricklefs 1998). Some details are described below.

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Fig. 1.

Fig. 1. The modified time calibrated Bayesian tree and a plot of fourmajor avian developmental modes (Prum et al. 2015). The complete tree is divided intoparts A and B. Scale in the Y-axis: millions of years ago.

Palaeognathae and Galloanserae are two oldest avian lineages and all of their membersbelong to the precocial developmental mode (Fig. 1). Neoaves include most of the livingbird lineages (Strisores, Columbaves, Gruiformes, Aequorlitornithes, and Inopinaces) (Fig.1). The most derived lineage, Inopinaves, belong to either the semialtricial or thealtricial mode. Opisthocomus hoazin is the only exception. It belongs tothe semiprecocial mode and is the most primitive Inopinaves (Fain and Houde 2004, Hackettet al. 2008, Jarvis et al. 2014). Therefore, our plotting implies that an altricialevolution event occurred after the emergence of Inopinaves.

In Neoaves, Strisores and Columbaves are two basal lineages and have terrestrial life.Strisores is peculiar in that, despite its early emergence, all its members belong toeither the semialtricial or altricial mode, implying that the earliest altricial modeevolution event occurred in this lineage. Columbaves encompasses all four developmentalmodes. Among Columbaves, two distinct clades (Cuculiformes and Columbiformes) belong tothe altricial mode, suggesting that at least two altricial mode evolution events occurredwithin this lineage.

The remaining two lineages, Gruiformes and Aequorlitornithes, are mostly water birds, orland birds without good flying ability. According to the phylogeny, Gruiformes could bebasal to Aequorlitornithes. All Gruiformes are water birds and belong to the precocialgroups, whereas Aequorlitornithes are highly diverse in their developmental mode.Interestingly, within Aequorlitornithes, the developmental mode evolved from precocialtoward altricial, resembling the whole avian evolutionary trend. At least one altricialevolution event occurred in this lineage.

In summary, the plotting suggests that at least five independent altricial modeevolutionary events occurred during modern avian evolution.

Trends of natal down evolution during avian evolution

Natal down is a diagnostic feature of the altricial-precocial spectrum. Natal down,evolved from environmental adaptation, provides insulation to keep hatchlings warm (Pap etal. 2017). However, the description of the downy plumage in bird hatchlings is stillscarce, not to mention the underlying molecular mechanism. Here we reviewed published datato construct a possible scenario of natal down evolution during avian evolution.

According to previous studies, the plumage differences between altricial and precocialbird hatchlings could be due to macropattern and micropattern changes in featherdevelopment (Chen et al. 2016). Feather macropattern, or pterylosis, is the feather tractdistribution of a bird (Fliniaux et al. 2004, Ho et al. 2019, Olivera-Martinez et al.2004). In feather tracts, the follicles of contour feathers are concentrated in densetracts called pterylae and are separated by bare areas called apteria (Fig. 2). Thefeather tract area is smaller in altricial birds than precocial birds, but the reason forthe divergence is still not clear. Three explanations have been proposed: (1) The apteriummay be an adaptation to reduce the total feather weight. (2) The movement of the body andthe feathers could be better accommodated by an increase in apterium. (3) The apterium mayaid birds in thermoregulation during flight or brooding (Chen et al. 2016, Stettenheim2015). In other words, flying ability contributes to the feather tract divergence andaltricial birds are usually better in flight. Our previous data showed that feather tractscover almost the entire body surface in chicken hatchlings, whereas in zebra finchhatchlings they only cover part of the body (Fig. 2) (Chen et al. 2016). This phenomenonimplies a relationship between feather macropatterning and avian evolution.

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Fig. 2.

Fig. 2. Schematic diagram of feather tract and types of natal downformation in zebra finch and chicken. Zebra finch embryos show two types of featherformation: Type I feather formation (open circles), in which the feather buds do notdevelop into downy feather; Type II feather formation (black circles), in which thefeather buds develop into downy feathers, which are later replaced by contourfeathers. Chicken embryos exhibit only the Type II feather formation. E8, E9, and E12:embryo day 8, 9 and 12, respectively. D7: 7 days post-hatch. Scale bar = 0.1 cm. Thefigure was modified from our previous study (Chen et al. 2017).

Feather micropatterning is the development of individual feather buds. Feather diversityappears in different body regions in adult birds and at developmental stages of a bird.For example, flight feathers enable the bird to fly, body contour feathers providephysical protection and shape the body outline, and down feathers keep the body warm. Ourprevious studies revealed regulatory differences among different body feathers or amongdifferent parts of a feather in chickens (Ng et al. 2014 2015, Wu et al. 2015). However,most bird hatchlings only show natal down and we found differences in natal down growthpatterns between the precocial chicken and altricial zebra finch, implying that feathermicropatterning contributed to avian evolution.

To address the contribution of micropatterning to avian evolution, we reviewed theliterature in natal down development. We considered four major developmental modes:precocial, semiprecocial, semialtricial, and altricial hatchlings. However, we found thatthe staging of semiprecocial bird embryos has never been characterized. Therefore, wefocused on natal down development of a basal precocial bird (emu), a semialtricial bird(pigeon), and an altricial sister clade of finch (parrot).

Emu, Dromaius novaehollandiae, is a member of Paleognathae, which alsoincludes other ground living birds: ostrich, rhea, tinamou, kiwi, and cassowary (Nagai etal. 2011). Paleognathae is the basal lineage of modern birds and all the members belong tothe precocial mode (Fig. 1). Compared to chicken hatchlings, emu hatchlings come fromlarger eggs, have a larger body size, require a longer incubation time, and developpeculiar limb types (Nagai et al. 2011). However, like chicken hatchlings, emu hatchlingsare covered with natal down throughout the body surface and can feed by themselves soonafter hatching (Nagai et al. 2011). These observations imply that precocial birds sharesimilar body natal down distribution and feeding behaviors. Strisores and Columbavesinclude the basal altricial and semialtricial lineages. Pigeon, Columbalivia, belongs to Columbaves, but its developmental mode is debated. Somestudies assign it as an altricial bird, while others classify it as a semialtricial bird(Dyke and Kaiser 2010, Łukasiewicz and Boruc 2014, Olea and Sandoval 2012, Starck andRicklefs 1998). Although pigeon hatchlings demand much parental care, in the literatureand our own breeding study, we found that natal down covers most of the body surface,except the posterior ventral region (Fig. 3). Therefore, by using natal down as theindicator, we classify the pigeon to the semialtricial mode.

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Fig. 3.

Fig. 3. Schematic diagram of bird hatchlings. Dorsal (upper row) andventral (lower row) views of chicken (precocial), pigeon (semialtricial), parrot(altricial) and zebra finch.

Zebra finch, Taeniopygia guttata, belongs to the most derived anddiverse bird lineage, Passerineform. All passerines are classified as altricial birds.Their hatchlings show no or sparse natal down on the body surface and demand much parentalcare. We found that zebra finch hatchlings have two types of feather formation. In thepterylae region, Type I feather buds grow contour feather directly from the follicleswithout going through the natal down; that is, the natal down follicle forms, but featherfilament does not. Type II feather buds, like the feather buds in precocial birds, developinto natal down feather filament and later grow contour feathers after replacing the nataldown in the same follicles (Chen et al. 2016). The contour feathers grow from both typesof feather buds at similar stages (D7, Fig. 2).

Parrot (Myiopsitta monachus), a sister clade to finch, is an altricialbird (Carril and Tambussi 2015, Prum et al. 2015). However, its natal down development isdifferent from that of zebra finch. According to previous studies and our observation, thehatchlings of both species show no natal down on ventral skin; on dorsal skin, zebra finchhatchlings show mature natal down, while parrot hatchlings show growing natal down,starting from naked-like hatchlings in newborns to downy feathers on dorsal skin in laterstages (Fig. 3). We can only find the Type I feather formation in the ventral region, andimmature natal down forms in the dorsal region of parrot hatchlings. Thus, the natal downgrowth pattern may differ between parrot and zebra finch.

By comparing the hatchlings of the above four avian species, we propose an evolutionaryscenario of natal down plumage evolution during avian evolution: natal down initiallycovered the entire body in precocial hatchlings. After precocial birds occupied most ofthe land niches, semiprecocial and semialtricial birds with better flight ability evolvedand extended their habitat to waters, oceans, or higher places. Semialtricial birds canbuild nests in hidden places. Therefore, their hatchlings can snuggle in the nest andtheir ventral natal downs are no longer necessary. Finally, altricial birds evolvedbecause they have higher intelligence and can build sophisticated nests, so the hatchlingsneeded less natal down and can re-allocate their saved energy to other organs, such asdigestive organs (Blom and Lilja 2005).

In summary, although natal down plumage is a diagnostic character to distinguish betweendevelopmental modes, it is not a simple diagnostic character because of the diversity insemiprecocial, semialtricical and altricical bird lineages. Further study in natal downplumage classifications is needed.

Molecular mechanisms of feather development

The source tissues for feather tract development are embryonic somatopleure and somite(Fliniaux et al. 2004). The proximal somatopleural mesoderm forms a feather-forming dermisat E2 (2 days of incubation) (Fliniaux et al. 2004). At the molecular level, likeHOX gene clusters that define the animal body plan, feathermacropatterns are defined by regional identity, and some regulators have been identified(Fliniaux et al. 2004, Ho et al. 2019, Houghton et al. 2005). The members of theectodysplasin pathway, Ectodysplasin A (EDA), Ectodysplasin A receptor (EDAR) andectodysplasin receptor associated death domain (EDARADD) are known to be involved in thepatterning and could be directed by β-catenin signaling and/or BMP2 (Bone morphogeneticproteins 2) (Ho et al. 2019, Houghton et al. 2005). During chicken early skin development(E6.5), the expanding expression of EDA imposes the travelling wave offeather formation. The EDA wave spreads across a mesenchymal cell densitygradient and lowers the threshold of mesenchymal cells required to begin the feather budformation, further triggering the pattern formation. Interestingly, such waves and theprecise arrangement of feather primordia are lost in the flightless emu and ostrich (Ho etal. 2019). In zebra finch, the expression pattern of EDA is unclear. Weobserved that the regular arrangement of feather primordia remains, but how the reducedfeather tract formed is still unclear (Chen et al. 2017).

Once feather tracts are established, the feather micropatterning is initiated. Fiveproperties, localized growth zone (LoGZ), invagin*tion, branching, feather β-keratin, anddermal papilla (stem cell), have been characterized in feathers (Fig. 4A) (Wu et al.2018). To localize the growth zone, the spatial arrangement and regular outgrowth offeathers are regulated by the epithelio-mesenchymal molecular interactions between thedermis and the overlying epidermis (Chen et al. 2015, Ho et al. 2019, Meinhardt and Gierer2000, Mou et al. 2011, Wells et al. 2012). Many molecules that act with the process havebeen identified. For example, WNT/b-catenin signaling and TWIST2 are promoters at theearly stages of skin patterning, not only for feather tract establishment but also forfeather growth initiation (Hornik et al. 2005, Noramly et al. 1999, Widelitz et al. 2000).Some FGFs (fibroblast growth factors) and SHH (sonic hedgehog) are promoters oractivators, while some BMPs (bone morphogenetic proteins) are inhibitors of featherplacode formation (Jung et al. 1998, Mandler and Neubuser 2004, McKinnell et al. 2004,Song et al. 2004). Branching formation within a feather filament is formed by invagin*tionof the multilayered filament epithelium surrounding the mesenchyme. This event takes placein the ramogenic zone, and NOTCH, FGF, GDF10 and GREM1 that modulate the BMP signalingwere reported to regulate the periodic-branching process (Cheng et al. 2018, Li et al.2017). Feather rachis is formed by the fusion of barb ridges at the anterior end of thefeather, and BMP, NOG, SPRY, and FGF are known to regulate the periodic invagin*tion thatforms barb and rachis (Chen et al. 2015, Chuong et al. 2014, Ng and Li 2018).

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Fig. 4.

Fig. 4. Five developmental stages of feathers and the regulators fornatal down growth suppression in zebra finch. (A) Schematic diagram shows the fivedevelopmental stages of feathers: LoGZ, invagin*tion, branching, feather β-keratin,and dermal papilla (Wu et al. 2018). (B) A summary of the mRNAs identified in Type Iand Type II feather formations in zebra finch (Chen et al. 2016).

Although the feather developmental process and the underlying regulators are largelyidentified, all the researches related to it only have been done in domestic chicken. Theregulatory mechanisms in diverse natal down growth in altricial birds are less studied.The genes underlying some chicken featherless mutants have been characterized. Theregulatory differences in BMPs cause the naked neck phenotype in chicken, and a nonsensemutation in FGF20 is associated with the featherless trait (Mou et al. 2011, Wells et al.2012). However, both chicken variants show no established feather buds on the nakedregion, unlike the Type I feather formation process we observed in zebra finch and parrot.By using comparative transcriptomics, we found that FGF16 and the mitogen-activatedprotein kinase (MAPK) signaling pathway are involved in natal down growth suppression inzebra finch (Fig. 4B) (Chen et al. 2016). However, how the regulation is achieved andwhether it has been conserved in altricial birds, or natal down suppressed birds, needfurther study.

CONCLUSIONS AND PERSPECTIVE

The altricial-precocial spectrum traditionally describes the developmental modes of mammalsand birds at birth (Augustine et al. 2019). The developmental modes are highly associatedwith parental care, habitat selection, and environmental adaptation. Natal down plumage isone of the indicators for the altricial-precocial spectrum and is strongly related to avianevolution. However, previous studies rarely described the natal down plumage precisely whenanalyzing the spectrum. In this review, we first plotted the altricial-precocial spectrum tothe recently published avian phylogeny to explore the evolution of the developmental modesduring avian evolution. We then focused on the natal down plumage differences inrepresentative precocial, semialtricial, and altricial birds to construct the probableevolutionary steps for natal down plumage degeneration. Finally, we reviewed the molecularmechanism for feather development and described the possible mechanisms involved in nataldown plumage diversification among birds.

The phylogeny of birds has been difficult to construct because of the rapid speciesradiation from the Cretaceous to Paleogene (K-Pg) (Jarvis et al. 2014). Jarvis et al. (2014)recently published a whole-genome- based avian phylogeny. However, species phylogenyconstruction relies not only on the sequencing coverage of the genome, but also on the nodesof the species. The avian phylogeny including all major avian lineages with lower genomesequencing coverage was constructed (Prum et al. 2015). Although the two phylogenetic treesshow some differences (for example, the position of birds of prey), both trees fit ourmodel. Here we adopt a phylogeny with a lower genome coverage but a larger node number asour analysis backbone (Prum et al. 2015). However, as large scale bird genome sequencing isprogressing rapidly, the phylogeny may soon be revised. A recent large scale genomic studyin passerines revealed their precise phylogeny and an interesting evolutionary trajectory,and a similar study in semiprecocial and semialtricial species will largely improve thestudy of evolution of the altricial- precocial spectrum (Oliveros et al. 2019). Moreover,the accumulation of the morphological data can also alter the phylogeny. Most morphologicaldata are from investigations and records from birds in the wild, so it is difficult to knowwhether the bird hatchlings were recorded at birth or several days after birth. We haveobserved that, at least in parrots, natal down grows vigorously after birth, so the spectrumshould be characterized at birth.

Feather development involves the interaction of numerous molecules. The major regulators atdifferent developmental stages were basically identified as mentioned above. However, howthose regulators are regulated in feather development is still unclear. The phenotypicchanges could have resulted from coding and/or non-coding sequence changes. Coding sequencevariation is known to be a key factor in domestic chicken variation (Mou et al. 2011, Ng andLi 2018, Ng et al. 2012, Wells et al. 2012). However, such cases have rarely been identifiedin wild birds, and non- coding sequence variation contributes more to the intra- speciesvariation (Küpper et al. 2016, Lamichhaney et al. 2015 2016). Indeed, despite the abundanceof bird species, their chromosomal structures have been surprisingly well conserved overevolutionary time (Frankl-Vilches et al. 2015, Skinner and Griffin 2012). Also, codingsequence evolution is relatively slower in birds than other vertebrates (Nam et al. 2010,Weber et al. 2014). Therefore, coding sequence variation should not be the majorevolutionary effector for bird diversity. Non-coding sequences can act as gene regulatoryregions, such as promoters and enhancers, or non- coding transcripts, such as non-codingRNAs. In mouse, regional specificity regulation has been characterized at the epigeneticlevel (Ezhkova et al. 2011, Fabre et al. 2017, Rodriguez-Carballo et al. 2017) and in non-coding RNA (Caley et al. 2010). Similar mechanisms may act in the avian genome, but furtherstudies will be needed.

Research on feather development and diversity expands our view of how complex structurescan evolve to increase an organism’s survival and persistence. However, the importance ofthe “natal down diversity”, in terms of their types and topological distribution, could havelong been underestimated. The evolution from precocial to altricial modes has been thoughtto be environmental adaptation. However, most of the diagnostic characters are difficult toqualify or quantify, so the spectrum evolution has been debated for a long time. Natal downis the only discrete character for the diagnosis, and our view in that altricial-precocialspectrum evolution is based on our characterization of different types and patterns of thenatal down. Furthermore, different developmental stages of bird exhibit different types offeather. Juvenile birds are ready to leave the nest and most natal downs are replaced bycontour feathers (Podulka et al. 2004), which enable the birds to fly. After moultingseveral times, more functional feathers are derived from the juvenile feather follicles toachieve specific functions in adult birds (Terres 1991, National Audubon Society), includingfeathers used in camouflage, migration, overwintering, or courtship (Dunn et al. 2011). Thehatchling (natal down) to juvenile (contour feather) plumage transition happens only once inmost birds, but the mechanism has never been characterized. A continuous investigation ofhatchling to juvenile plumage change will further help us explore the mystery of evolutionfrom precocial to altricial modes in birds.

Acknowledgments

Acknowledgment: We thank Drs Ping Wu and Cheng Ming Chuong for theirsuggestions and for permission to use the feather development model. We thank Dr. RichardPrum for his permission to use of the phylogenetic tree. This study was supported by MOST,Taiwan (MOST 107-2311-B-001-016-MY3).

Footnotes

Authors’ contributions: C.-C.K. and W.-H.L. designed the research; C.-C.K.,S.-M.W., and H.-F.C. performed the research and analyzed the data; and C.-C. K. andW.-H.L. wrote the paper.

Competing interests: The authors declare no competing interests.

Availability of data and materials: The datasets used and analyzed duringthe current study are available from the first or corresponding author on request.

Ethics approval consent to participate: All the data were downloaded fromthe internet.

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