Kiwi genome provides insights into evolution of a nocturnal lifestyle

Abstract

BackgroundKiwi, 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.ResultsWe 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.ConclusionsThe 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-015-0711-4) contains supplementary material, which is available to authorized users.

Adaptation to nocturnality – learning from avian genomes

“…The result of such analyses (comparative genomics and gene ontology analyses) is typically a list of processes or functions (for example metabolic pathways) that are significantly associated with, for example, nocturnality. For example, many comparative genomics studies have revealed a higher diversification of the olfactory receptors repertoire . Although this is an expected biological trait, the unbiased result of comparative genomics offers further support to the importance of olfaction in low‐light environments.…”

“…). To detect changes that are relevant for adaptation to nocturnality, one can make use of already assembled bird genomes and compare nocturnal versus diurnal species (Fig. ).…”

The value of new genome references

“…In the honey bee and other eusocial bees genetic pathways that control DNA methylation are found that are not present in drosophila, and DNA methylation is used to regulate the reproductive suppression of worker bees[13–15]. Combinations in these innovations may indicate a shift in species ecology such as the kiwi, where opsin genes related to color vision are inactivated and the odorant receptor repertoire is expanded, consistent with increased reliance on olfaction for nocturnal foraging[16]. Perhaps the most dramatic example of massive expansion and diversification is that of animal parasitic effector genes to avoid recognition by the plant immune system.…”

Conservation physiology can inform threat assessment and recovery planning processes for threatened species

“…Young are released into a predator-free zone to learn effective foraging techniques prior to release into the wild as adults (Robertson et al 2011). Genetics of the reared kiwis determine where they are released as adults to ensure genetic diversity and survival (Colbourne et al 2005, Le Duc et al 2015. This translocation program informed by physiological data has aided in the reclassification of 2 kiwi species to Vulnerable, and a third species to Near Threatened (IUCN 2016).…”