Disentangling the evolutionary history and biogeography of hill partridges (Phasianidae, Arborophila) from low coverage shotgun sequences

Highlights

• A phylogenomic analysis of the galliform genus Arborophila is presented.

• 14 of 15 Arborophila species were analyzed, six were from museum specimens.

• Various data types extracted from mapping from low coverage shotgun sequencing.

• Their evolution was influenced by geological and climatic events in Southeast Asia.

Abstract

The advent of the phylogenomic era has significantly improved our understanding of the evolutionary history and biogeography of Southeast Asia’s diverse avian fauna. However, the taxonomy and phylogenetic relationships of many Southeast Asian birds remain poorly resolved, especially for those with large geographic ranges, which might have experienced both ancient and recent geological and environmental changes. In this study, we examined the evolutionary history and biogeography of the hill partridges (Galliformes: Phasianidae: Arborophila spp.), currently the second most speciose galliform genus, and thought to have colonized Southeast Asia from Africa. We present a well‐resolved phylogeny of 14 Arborophila species inferred from ultra-conserved elements, exons, and mitochondrial genomes from both fresh and museum samples, which representing almost complete coverage of the genus. Our fossil-calibrated divergence time estimates and biogeographic modeling showed the ancestor of Arborophila arrived in Indochina during the early Miocene, but the initial divergence within Arborophila did not occur until ~10 Ma when global cooling intensified. Subsequent dispersal and diversification within Arborophila were driven by several tectonic and climatic events. In particular, we found evidence of rapid radiation in Indochinese Arborophila during the Pliocene global cooling and extensive dispersal and speciation of Sundaic Arborophila during the Pleistocene sea-level fluctuations. Taken together, these results suggest that the evolutionary history and biogeography of Arborophila were influenced by complex interactions among historical, geological and climatic events in Southeast Asia.

Introduction

Southeast Asia hosts extremely high species richness of terrestrial taxonomic groups (Myers et al., 2000, Sodhi et al., 2004), especially for birds (Jetz et al., 2012, Jetz et al., 2014). Studies on the origin and evolution of birds in Southeast Asia have long been a hot topic since Alfred Russel Wallace (e.g., Lohman et al., 2011, Päckert et al., 2012). Recent studies suggest that tectonic and climatic events form the major drivers for the origin and evolution of the remarkable avian components and richness in Southeast Asia (Sheldon et al., 2015). For examples, ancient tectonic events with the associated climatic changes allowed taxa originating in Laurasia (e.g., Coraciiformes and Trogonidae; Andersen et al., 2018, Oliveros et al., 2019a), the Australian landmass (e.g., Passeriformes, Psittaciformes, Columbiformes; Cibois et al., 2017, Moyle et al., 2016, Oliveros et al., 2019b, Schweizer et al., 2010) and Africa (e.g., Galliformes and Bucerotidae; Cai et al., 2018, Gonzalez et al., 2013) to disperse into Southeast Asia. And more recently, Pleistocene sea-level fluctuations caused islands in Southeast Asia to repeatedly sunder and fuse with each other and/or the mainland, which facilitated divergences among populations and closely related species across islands and mainland that are currently separated (e.g., Lohman et al., 2011, Rheindt et al., 2020, Woodruff, 2010). Although these higher-level phylogenetic and population-level phylogeographic studies have significantly improved our knowledge on the evolution of Southeast Asia’s avian fauna, few studies have undertaken species-level phylogeny of particular taxonomic groups that have experienced both ancient and recent tectonic and climatic events (but see den Tex and Leonard, 2013). The hill partridges (Arborophila) are thought to be an early colonizer into Southeast Asia from Africa and is currently speciose (Crowe et al., 2006, del Hoyo et al., 2019, Madge and McGowan, 2002), making it an ideal group to study and disentangle the effect of both ancient and recent tectonic and climatic changes on the diversification of Southeast Asian birds.

The hill partridges are a genus of small, rotund galliforms. They are currently distributed in the forests of the Sundaic region (Borneo, Sumatra, Java, and the Malay Peninsula), Indochina, the Himalayas, Hengduan Mountains, South China and Taiwan island (Johnsgard, 1988, Madge and McGowan, 2002; Fig. 1). Previous studies showed that Arborophila and other Sundaic partridges (i.e., Caloperdix, Rollulus, and Melanoperdix) are phylogenetically closer to the African partridge genus Xenoperdix (Crowe et al., 2006, Hosner et al., 2016b, Wang et al., 2017b). These cross-continent relationships were thought to have originated from dispersal events between Africa and Asia during the late Oligocene (Sheldon et al., 2015, Wang et al., 2017b). Arborophila is the second largest genus within the order Galliformes after the African francolin genus Pternistis (del Hoyo et al., 2019). It contains 15–19 species after excluding members of the recently revived genus Tropicoperdix (Chen et al., 2015a, Gill and Donsker, 2019). Different taxonomic treatments on two species complex, A. orientalis–sumatrana–campbelli–rolli and A. cambodiana–diversa, lead to the varied recognition of species-level taxonomic changes (Davison, 1982, del Hoyo et al., 2019, Gill and Donsker, 2019, Madge and McGowan, 2002). However, setting aside these taxonomic uncertainties surrounding the two species complex, the phylogeny of the 15 taxonomically uncontroversial species has so far been poorly investigated. Earlier hypotheses on the interspecific relationships within Arborophila have been mainly based on plumage similarities (Cheng, 1978, Davison, 1982, Johnsgard, 1988), which were subsequently weakened by more recent molecular phylogenies (Wang et al., 2013; Fig. S1). Until now, fewer than ten Arborophila species have been available for molecular phylogenetic analyses, and the hypothesized relationships have varied among different studies (e.g., Chen et al., 2015a, Wang et al., 2013, Yan et al., 2017). The low species coverage and inconsistent phylogenetic relationships of existing studies have thus hindered our understanding of the evolutionary history of Arborophila and the potential roles of geological shifts and climate fluctuations in the diversification and biogeography of this speciose genus.

Hill partridges are cryptic undergrowth dwellers of tropical and subtropical forest, with sedentary habits (Madge and McGowan, 2002). The populations of many hill partridge species are in decline due to the on-going habitat loss and five species are listed as threatened species by the International Union for Conservation of Nature (IUCN, 2019). It is thus challenging to obtain fresh samples. Natural history museum collections are valuable repositories for evolutionary and phylogenetic studies and next-generation DNA sequencing (NGS) provides feasible ways to obtain orthologous loci from museum specimens (Bi et al., 2013). Sequence capture and low coverage shotgun sequencing are two commonly used NGS methods for phylogenetic questions from museum specimens (e.g., Chen et al., 2018, McCormack et al., 2016), and low coverage shotgun sequencing can yield comparable amounts of different types of orthologous loci (e.g., UCEs, exons, mitochondrial genomes) (Chen et al., 2018).

In this study, we examined the molecular phylogeny for 14 of 15 taxonomically uncontroversial Arborophila species based on genome-wide genetic markers including ultraconserved elements (UCEs), exons, and mitochondrial genomes. After determining the phylogenetic relationships, we conducted molecular dating and ancestral area reconstruction to infer the evolutionary and biogeographic histories of Arborophila. Through these efforts, our results clearly showed that the evolution of Arborophila was affected by a series of both ancient and recent, global and regional tectonic and climatic events.