Multilocus phylogeny of the avian family Alaudidae (larks) reveals complex morphological evolution, non-monophyletic genera and hidden species diversity

Abstract

The Alaudidae (larks) is a large family of songbirds in the superfamily Sylvioidea. Larks are cosmopolitan, although species-level diversity is by far largest in Africa, followed by Eurasia, whereas Australasia and the New World have only one species each. The present study is the first comprehensive phylogeny of the Alaudidae. It includes 83.5% of all species and representatives from all recognised genera, and was based on two mitochondrial and three nuclear loci (in total 6.4 kbp, although not all loci were available for all species). In addition, a larger sample, comprising several subspecies of some polytypic species was analysed for one of the mitochondrial loci. There was generally good agreement in trees inferred from different loci, although some strongly supported incongruences were noted. The tree based on the concatenated multilocus data was overall well resolved and well supported by the data.We stress the importance of performing single gene as well as combined data analyses, as the latter may obscure significant incongruence behind strong nodal support values. The multilocus tree revealed many unpredicted relationships, including some non-monophyletic genera (Calandrella, Mirafra, Melanocorypha, Spizocorys). The tree based on the extended mitochondrial data set revealed several unexpected deep divergences between taxa presently treated as conspecific (e.g. within Ammomanes cinctura, Ammomanes deserti, Calandrella brachydactyla, Eremophila alpestris), as well as some shallow splits between currently recognised species (e.g. Certhilauda brevirostris-C. semitorquata-C. curvirostris; Calendulauda barlowi-C. erythrochlamys; Mirafra cantillans-M. javanica). Based on our results, we propose a revised generic classification, and comment on some species limits. We also comment on the extraordinary morphological adaptability in larks, which has resulted in numerous examples of parallel evolution (e.g.

A review of the recent advances in the systematics of the avian superfamily Sylvioidea

“…Recent studies have revealed considerable hidden diversity in some taxa, such as Mirafra assamica, which was proposed to be split into four species based mainly on vocal, behavioral and morphological data (Alström, 1998; corroborated by molecular study by Alström et al, 2013); the Calendulauda (previously Certhilauda) albescens complex, which was suggested to consist of three instead of two species based on mitochondrial, morphological and vocal data (Ryan et al, 1998); the Certhilauda curvirostris complex, which was recommended to be treated as five instead of one species based on mitochondrial and morphological evidence (Ryan and Bloomer, 1999); and Galerida cristata, which was shown to consist of two partly sympatric and largely reproductively isolated species in Morocco, G. cristata sensu stricto and G. macrorhyncha (Guillaumet et al, 2005(Guillaumet et al, , 2006(Guillaumet et al, , 2008. In an analysis of mitochondrial data, Alström et al (2013) found several unexpectedly deep divergences between taxa presently treated as conspecific (e.g. within Ammomanes cinctura, Ammomanes deserti, Calandrella brachydactyla, Eremophila alpestris), but also some shallow splits between currently recognized species (e.g.…”

“…However, a phylogeny including 81 of the 97 species and representatives of all 21 recognized genera, based on two mitochondrial and three nuclear loci has just appeared (Alström et al, 2013). The latter has revealed many unpredicted relationships, including some non-monophyletic genera (Calandrella, Mirafra, Melanocorypha, Spizocorys), and proposed a revised generic classification.…”

“…C. rufescens and C. cheleensis) are more closely related to a clade containing the two monotypic genera Eremalauda and Chersophilus; the close affinity between Eremalauda and Chersophilus was also totally unexpected. Alström et al (2013) proposed that the name Alaudala be used for the second of these traditional Calandrella clades. Another surprising result from Alström et al's (2013) multilocus analysis was that Melanocorypha leucoptera and M. mongolica are not closely related, hence it was proposed that the former be moved to the genus Alauda.…”

“…Olsson et al (2013a) classified these clades as Eremomelinae, Cisticolinae, Priniinae and Neomixinae, Fig. 2 Family Cisticolidae based on concatenated nuclear MB and ODC and mitochondrial cytochrome b and ND2, based on Olsson et al (2013). Posterior probabilities (above) and maximum likelihood bootstrap (below) values are indicated at the nodes; an asterisk represents posterior probability 1.00 or maximum likelihood bootstrap 100%.…”

Complete mitochondrial genome of the Mongolian lark, Melanocorypha mongolica (Aves: Passeriformes)

“…Mitochondrial genomes have become the most widely used molecular markers among a broad array of molecular evolutionary and phylogenetic studies (Rong et al 2016). Several molecular phylogeny of the Alaudidae has been published, based on mitochondrial and nuclear sequences from mostly larks species (Tieleman et al 2003;Alstr€ om et al 2013). However, only one complete mitochondrial genome, Eurasian Skylark Alauda arvensis (under accession no.JQ322641, Qian et al 2013), is available in GenBank.…”