Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2015 Jul 23;16(1):147.
doi: 10.1186/s13059-015-0711-4.

Kiwi Genome Provides Insights Into Evolution of a Nocturnal Lifestyle

Affiliations
Free PMC article

Kiwi Genome Provides Insights Into Evolution of a Nocturnal Lifestyle

Diana Le Duc et al. Genome Biol. .
Free PMC article

Abstract

Background: Kiwi, comprising five species from the genus Apteryx, are endangered, ground-dwelling bird species endemic to New Zealand. They are the smallest and only nocturnal representatives of the ratites. The timing of kiwi adaptation to a nocturnal niche and the genomic innovations, which shaped sensory systems and morphology to allow this adaptation, are not yet fully understood.

Results: We sequenced and assembled the brown kiwi genome to 150-fold coverage and annotated the genome using kiwi transcript data and non-redundant protein information from multiple bird species. We identified evolutionary sequence changes that underlie adaptation to nocturnality and estimated the onset time of these adaptations. Several opsin genes involved in color vision are inactivated in the kiwi. We date this inactivation to the Oligocene epoch, likely after the arrival of the ancestor of modern kiwi in New Zealand. Genome comparisons between kiwi and representatives of ratites, Galloanserae, and Neoaves, including nocturnal and song birds, show diversification of kiwi's odorant receptors repertoire, which may reflect an increased reliance on olfaction rather than sight during foraging. Further, there is an enrichment of genes influencing mitochondrial function and energy expenditure among genes that are rapidly evolving specifically on the kiwi branch, which may also be linked to its nocturnal lifestyle.

Conclusions: The genomic changes in kiwi vision and olfaction are consistent with changes that are hypothesized to occur during adaptation to nocturnal lifestyle in mammals. The kiwi genome provides a valuable genomic resource for future genome-wide comparative analyses to other extinct and extant diurnal ratites.

Figures

Fig. 1
Fig. 1
Phylogenetic tree of 16 species built on 623 TreeFam [12] single-gene families. Branch lengths are scaled to estimate divergence times. All branches are supported by 100 bootstraps. The song bird clade is depicted in blue, Galliformes jn purple, Anseriformes in green, and nocturnal birds in red. Ratites (Struthio camelus and Apteryx mantelli) and Tinamus guttatus are highlighted in light green. The number of genes gained (+ red) and lost (− blue) is given underneath each branch. The rate of gene gain and loss for the clades derived from the most common recent ancestor was estimated [77] to 0.0007 per gene per million years
Fig. 2
Fig. 2
Protein sequence comparison revealed substitutions of Glu3.49 to Lys (E/DRY motif) and Glu6.30 to Gly in kiwi OPN1MW (RH2) and kiwi OPN1SW, respectively. Both residues are 100 % conserved in all birds sequenced so far and over 100 publicly available sequences of other vertebrate OPN1MW and OPN1SW orthologs. To assure the OPN1MW-change is kiwi-specific additional ratites were sequenced, including different kiwi species and the extinct moa. Glu3.49 of the E/DRY motif and Glu6.30 at the N-terminal end of helix 6 are parts of an ‘ionic lock’ interhelical hydrogen-bond network which is highly conserved in many rhodopsin-like GPCRs. Nb – North Island brown kiwi, Ob – Okarito brown kiwi, Gs – Great spotted kiwi, Ec – Emeus crassus (Eastern moa), Pg – Pachyornis geranoides (Mappin’s moa), Chuck-will – Chuck-will’s-widow
Fig. 3
Fig. 3
Maximum likelihood (ML) tree constructed using full-length intact α and γ group olfactory receptors from 10 birds (chicken, zebra finch, flycatcher, duck, turkey, chuck-will’s-widow, barn owl, ostrich, tinamou, and kiwi) and two reptile genomes (anole lizard and Chinese soft-shell turtle). The ML topology shown above was cross-verified using the neighbor joining (NJ) method. Three Class A (Rhodopsin) family GPCRs from chicken genome, dopamine receptor D1 (DRD1), dopamine receptor D2 (DRD2), and histamine receptor H1 (HRH1) were used as the out-group (shown as non-olfactory receptors). The red dot indicates confidence estimates (% bootstrap from 500 resamplings, >90 % bootstrap support from both ML and NJ methods) for the nodes that distinguish α and γ ORs. The scale bar represents the number of amino-acid substitutions per site. The topology supports lineage specific expansions of γ group olfactory genes in the bird and the reptile species. Note, a few of the γ group ORs in kiwi cluster with reptilian ORs (highlighted by orange arrowhead), while some cluster basal to the clade containing bird ORs (highlighted by green arrowhead). The topology supports contrasting evolutionary rates within the analyzed γ ORs, as indicated by short (blue arc with arrowheads) and long branch lengths (pale orange arc with arrowheads). The inset shows the number of intact olfactory receptors in each species that are analyzed using the ML tree topology

Similar articles

See all similar articles

Cited by 16 articles

See all "Cited by" articles

References

    1. Bunce M, Worthy TH, Phillips MJ, Holdaway RN, Willerslev E, Haile J, et al. The evolutionary history of the extinct ratite moa and New Zealand Neogene paleogeography. Proc Natl Acad Sci U S A. 2009;106:20646–51. doi: 10.1073/pnas.0906660106. - DOI - PMC - PubMed
    1. Iviartin GR. Sensory capacities and the nocturnal habit of owls (Strigiformes) IBIS. 1986;128:266–77.
    1. Corfield JR, Parsons S, Harimoto Y, Acosta ML. Retinal anatomy of the New Zealand kiwi: structural traits consistent with their nocturnal behavior. Anat Rec (Hoboken) 2015;298:771–9. doi: 10.1002/ar.23080. - DOI - PubMed
    1. Gerkema MP, Davies WI, Foster RG, Menaker M, Hut RA. The nocturnal bottleneck and the evolution of activity patterns in mammals. Proc Biol Sci. 2013;280:20130508. doi: 10.1098/rspb.2013.0508. - DOI - PMC - PubMed
    1. Kelley DR, Schatz MC, Salzberg SL. Quake: quality-aware detection and correction of sequencing errors. Genome Biol. 2010;11:R116. doi: 10.1186/gb-2010-11-11-r116. - DOI - PMC - PubMed

Publication types

LinkOut - more resources

Feedback