A novel mitochondrial genome of Arborophila and new insight into Arborophila evolutionary history

Abstract

The lineage of the Bar-backed Partridge (Arborophila brunneopectus) was investigated to determine the phylogenetic relationships within Arborophila as the species is centrally distributed within an area covered by the distributions of 22 South-east Asian hill partridge species. The complete mitochondrial genome (mitogenome) of A. brunneopectus was determined and compared with four other hill partridge species mitogenomes. NADH subunit genes are radical in hill partridge mitogenomes and contain the most potential positive selective sites around where variable sites are abundant. Together with 44 other mitogenomes of closely related species, we reconstructed highly resolved phylogenetic trees using maximum likelihood (ML) and Bayesian inference (BI) analyses and calculated the divergence and dispersal history of Arborophila using combined datasets composed of their 13-protein coding sequences. Arborophila is reportedly be the oldest group in Phasianidae whose ancestors probably originated in Asia. A. rufipectus shares a closer relationship with A. ardens and A. brunneopectus compared to A. gingica and A. rufogularis, and such relationships were supported and profiled by NADH dehydrogenase subunit 5 (ND5). The intragenus divergence of all five Arborophila species occurred in the Miocene (16.84~5.69 Mya) when there were periods of climate cooling. We propose that these cooling events in the Miocene forced hill partridges from higher to lower altitudes, which led to geographic isolation and speciation. We demonstrated that the apparently deleterious +1 frameshift mutation in NADH dehydrogenase subunit 3 (ND3) found in all Arborophila is an ancient trait that has been eliminated in some younger lineages, such as Passeriformes. It is unclear of the biological advantages of this elimination for the relevant taxa and this requires further investigation.

About the Authors:

Chaochao Yan

Roles Conceptualization, Data curation, Formal analysis, Investigation, Software, Visualization, Writing – original draft, Writing – review & editing

Affiliation: Key Laboratory of Bio-Resources and Eco-Environment (Ministry of Education), College of Life Sciences, Sichuan University, Chengdu, P.R. China

ORCID http://orcid.org/0000-0003-1237-8978

Biqin Mou

Roles Data curation, Formal analysis, Investigation, Visualization

Affiliation: Key Laboratory of Bio-Resources and Eco-Environment (Ministry of Education), College of Life Sciences, Sichuan University, Chengdu, P.R. China

Yang Meng

Roles Formal analysis, Investigation

Affiliation: Key Laboratory of Bio-Resources and Eco-Environment (Ministry of Education), College of Life Sciences, Sichuan University, Chengdu, P.R. China

Feiyun Tu

Roles Conceptualization, Methodology

Affiliations Key Laboratory of Bio-Resources and Eco-Environment (Ministry of Education), College of Life Sciences, Sichuan University, Chengdu, P.R. China, Institute of Wildlife Conservation, Jiangxi Academy of Forestry, Nanchang, P.R. China

Zhenxin Fan

Roles Conceptualization, Project administration

Affiliation: Sichuan Key Laboratory of Conservation Biology on Endangered Wildlife, College of Life Sciences, Sichuan University, Chengdu, P.R. China

Megan Price

Roles Writing – review & editing

Affiliation: Sichuan Key Laboratory of Conservation Biology on Endangered Wildlife, College of Life Sciences, Sichuan University, Chengdu, P.R. China

Bisong Yue

Roles Funding acquisition, Supervision

Affiliation: Sichuan Key Laboratory of Conservation Biology on Endangered Wildlife, College of Life Sciences, Sichuan University, Chengdu, P.R. China

Xiuyue Zhang

Roles Conceptualization, Writing – review & editing

* E-mail: [email protected]

Affiliation: Key Laboratory of Bio-Resources and Eco-Environment (Ministry of Education), College of Life Sciences, Sichuan University, Chengdu, P.R. China

ORCID http://orcid.org/0000-0002-9681-2905

Introduction

Species of the Arborophila (commonly: hill partridge) are found in Asia from the Himalayas eastwards to Taiwan and south to Java. Arborophila is a very diverse genus, being the second most species rich genus within Galliformes [1–3]. Hill partridges are fairly small and their body typically ranges between 24 and 30 cm, while their beaks and tails are of equal length [2]. These small partridges are often brightly marked, but this marking provides camouflage in the leaf litter of eastern and southern Asia forests. Hill partridges are plump-bodied with thick necks and moderately long legs, stronger and longer tarsometatarsal, and rounded and rather short wings. Thus hill partridges are poor fliers with low aerial maneuverability.

The Arborophila genus contains over 20 species with 10 of those being found in China [2,4]. In 1998, eight of the 10 Chinese hill partridge species were listed in the China red data book of endangered animals as ‘Rare’ or ‘Endangered’ [5,6], among which the Sichuan Hill Partridge (A. rufipectus) and Hainan Partridge (A. ardens) are currently ranked as Endangered and Vulnerable, respectively, by IUCN Red List of Threatened Species [6]. Although some of the hill partridge species have a relatively wide distribution and inhabit a variety of habitats, their poor flying ability and ground-dwelling nature makes them vulnerable to human activities, non-indigenous predators and rapid loss of habitat and are thus rare within their respective ranges.

Research regarding the taxonomic status and interspecific relationships of Arborophila, is still in its infancy and is currently being debated [7–9]. Recent studies tend to place the Arborophila near the root position of Phasianidae [3,10–12], however, the phylogenetic relationship within Arborophila has been little studied.

Mitochondrial DNA (mtDNA) has frequently and widely been used as an ideal marker to resolve intractable phylogenies, because it typically accumulates mutations at a faster rate than nuclear DNA [8]. The accumulation of mutations makes it more effective to resolve relationships among recently diverged species or populations. However this rapid accumulation of mutations makes mtDNA incompatible to resolve older relationships because the more variable DNA sequences from remote species can easily become saturation [13]. Therefore we applied careful testing to avoid saturation occurring in our dataset. Another limitation of mtDNA is that it is considered prone to introgression among species and only reflects a one-sided perspective on the ancestry [14]. However, mtDNA has merits such as lack of recombination and is easily accessible. Moreover, the high rates of anatomical evolution match the rapid mitoDNA evolution in birds somehow[4,15–17].

Unlike the phylogenic distribution of Arborophila, the geographic distribution is relatively well understood. The widely distributed Bar-backed Partridge (A. brunneopectus) ranges across an area that sits centrally to the distributions of 22 extant hill partridge species, and overlaps with three of the 22 species (Fig 1). It is reported that A. brunneopectus shares a closer relationship with A. ardens, although the number of intermediate species between A. brunneopectus and A. ardens is unknown. Complete ecological data of these species are lacking [18–20].

[Figure omitted. See PDF.]

Fig 1. Geographic distribution of the five hill partridges within this study in comparison to the overall distribution of the other 17 hill partridges in South-east Asia.

The five studied hill partridge distributions have been assigned different colors while the others 17 are all colored midnight blue. Elevation information (altitude: meters above sea level) is represented by different heat colors.

https://doi.org/10.1371/journal.pone.0181649.g001

To date, only four mitogenomes within the genus Arborophila have been determined, while two are incomplete and lackspecific descriptions [21]. In this study, we determined the complete mitochondrial genome of A. brunneopectus. We also reconstructed the phylogenetic tree of 45 related birds and estimated contributions of every single mitogene to the consensus tree. Based on the divergence time and biogeographic data of the studied species, a hypothesis model of settlement and migration of hill partridge species was proposed. We also examined and discussed the relationship of variable sites and positive selective sites as well as the +1 frameshift mutation in NADH dehydrogenase subunit 3 (ND3) through the mitochondrial DNA alignments. The publication of the mitogenome of A. brunneopectus will greatly contribute to understanding of relationships within Arborophila.

Citation: Yan C, Mou B, Meng Y, Tu F, Fan Z, Price M, et al. (2017) A novel mitochondrial genome of Arborophila and new insight into Arborophila evolutionary history. PLoS ONE 12(7): e0181649. https://doi.org/10.1371/journal.pone.0181649

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