Wu et al. BMC Ecol Evo (2021) 21:162 BMC Ecology and Evolution https://doi.org/10.1186/s12862-021-01888-5 RESEARCH ARTICLE Open Access Genomic bases underlying the adaptive radiation of core landbirds Yonghua Wu1* , Yi Yan1, Yuanqin Zhao1, Li Gu1, Songbo Wang2 and David H. Johnson3* Abstract Background: Core landbirds undergo adaptive radiation with diferent ecological niches, but the genomic bases that underlie their ecological diversifcation remain unclear. Results: Here we used the genome-wide target enrichment sequencing of the genes related to vision, hearing, language, temperature sensation, beak shape, taste transduction, and carbohydrate, protein and fat digestion and absorption to examine the genomic bases underlying their ecological diversifcation. Our comparative molecular phy- loecological analyses show that diferent core landbirds present adaptive enhancement in diferent aspects, and two general patterns emerge. First, all three raptorial birds (Accipitriformes, Strigiformes, and Falconiformes) show a con- vergent adaptive enhancement for fat digestion and absorption, while non-raptorial birds tend to exhibit a promoted capability for protein and carbohydrate digestion and absorption. Using this as a molecular marker, our results show relatively strong support for the raptorial lifestyle of the common ancestor of core landbirds, consequently suggest- ing a single origin of raptors, followed by two secondary losses of raptorial lifestyle within core landbirds. In addition to the dietary niche, we fnd at temporal niche that diurnal birds tend to exhibit an adaptive enhancement in bright- light vision, while nocturnal birds show an increased adaption in dim-light vision, in line with previous fndings. Conclusions: Our molecular phyloecological study reveals the genome-wide adaptive diferentiations underlying the ecological diversifcation of core landbirds. Keywords: Gene capture, Convergent evolution, Raptor, Digestion, Ancestral trait reconstruction Background Falconiformes), which share many raptorial-lifestyle Core landbirds (Telluraves) is the recently defned larg- characteristics, similar selections may have occurred est clade in Neoaves, including raptors, woodpeckers, between them [5]. Despite their ecological similarities, parrots, and songbirds [1–3]. Core landbirds adapt to phylogenetic analyses show that the three birds of prey diverse environments with diferent phenotypes related are relatively distantly related, and it remains unknown to diets, diel activity patterns, language and hearing, etc. whether their similar raptorial lifestyles are a result of [4]. Adapting to diverse environments, diferent core single origin [2, 3] or multiple origin [1]. landbirds may have been subjected to divergent selec- Te Avian Phylogenomics Project evaluates the tions, whereas for ecologically similar taxa, for instance, genomic evolution of 48 avian species within the class three birds of prey (Accipitriformes, Strigiformes, and Aves with relatively little detailed analyses of genomic diference among avian subgroups, such as core landbirds [6]. Other comparative genomic or transcriptomic stud- *Correspondence: [email protected]; [email protected] ies related to core landbirds are restricted to specifc taxa 1 School of Life Sciences, Northeast Normal University, Changchun 130024, China [7–13] or specifc genes related to vision and digestion 3 Global Owl Project, 6504 Carriage Drive, Alexandria, VA 22310, USA [14–16]. A recent study of 16 genomes of birds of prey Full list of author information is available at the end of the article reveals their shared genetic adaptation underlying their © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Wu et al. BMC Ecol Evo (2021) 21:162 Page 2 of 14 anatomical structures and sensory, muscle, circulatory, followed the MPE approach and used likelihood ratio and respiratory systems related to a raptorial lifestyle tests based on branch and branch-site models imple- [5]. Despite these eforts, a more comprehensive study mented in the Codeml program of PAML [23] to identify with a sufcient sampling across both diferent taxa and positively selected genes (PSGs) along branches lead- functionally diferent genes is needed to better elucidate ing to diverse core landbird taxa. In addition to PAML, the integrative evolution of core landbirds in adapting to we employed the program RELAX [24] to examine the diverse ecological environments. selection strength changes (e.g., intensifed or relaxed) of Te recent development of a molecular phyloecologi- genes for our focal taxa. cal (MPE) approach, which employs a comparative phy- logenetic analysis of biologically meaningful genes, has been demonstrated to have power to reveal the genetic Selection analyses of the genes related to senses, bases that underlie phenotypic diferentiations and ena- language, beak and temperature ble ancestral trait reconstruction [17, 18]. In light of the To examine the molecular bases of phenotypic diferen- MPE approach, we in this study use target enrichment tiations of core landbird taxa, we initially constructed a sequencing to obtain gene sequences to examine the dataset by combining the captured coding sequences of genetic bases that underlie the ecological diversifcation our 46 taxa with the sequence data of 33 core landbird of core landbirds. Target enrichment sequencing has species available from GenBank (Fig. 1, Additional fle 3: been widely used in gene capture across species [19–22]. Table S3), referred to as the core landbird dataset here- Our comparative analyses show that diferent core land- after. Based on the core landbird dataset, we frstly used bird taxa exhibit taxon-specifc adaptations, whereas PAML to examine the adaptive evolution of the 33 genes ecologically similar taxa present somewhat similar evolu- involved in the phototransduction pathway (Fig. 2, Addi- tionary adaptations. Our study reveals the genomic bases tional fles 4, 5: Tables S4, 5), which have been used as underlying the adaptive radiation of core landbirds and the molecular markers to determine the diel activity pat- provides insights into the evolutionary history of their terns of birds and mammals [17, 18]. We found fve PSGs ecological diversifcation. (GRK1, LW S, RH2, SWS2, and ARR3) along the branch leading to Strigiformes (owls), which are mainly crepus- Results cularly and nocturnally active. GRK1 is a rod-expressed We used target enrichment sequencing to obtain the gene and is involved in the inactivation of activated rho- coding sequences of 308 genes related to vision, hear- dopsin, contributing to photoresponse recovery in dim- ing, language, temperature sensation, beak shape, taste light conditions. LW S, RH2, and SWS2, respectively, transduction, and carbohydrate, protein and fat diges- encode red-, green-, and blue-sensitive cone opsins, tion and absorption (Additional fle 1, Table S1; Addi- and their positive selections in owls are linked to spec- tional fle 13) from 46 core landbird taxa with an address tral tuning to maximize light abortion under crepus- on the sampling of birds of prey (Fig. 1, Additional fle 2: cular conditions, as previously evidenced [16]. ARR3 is Table S2), for which there are only sparse genome data involved in the inactivation of cone opsins for photore- available thus far. For the target enrichment sequencing sponse recovery. Moreover, we did not fnd any cap- of our focal 308 genes, we designed baits based on the tured sequences of violet- or ultraviolet-sensitive opsin coding sequences of these genes from multiple divergent gene (SWS1) from all 28 owl species examined, and this species (e.g., falcon, eagle and owl), which has been dem- was consistent with previous studies that consistently onstrated to be a highly efective strategy for increasing show the absence of the gene expression or sequence of capture efciency [22]. We then employed the same set SWS1 in owls [8, 9, 14, 16]. In addition to Strigiformes, of baits to capture and sequence our target genes across we found PSGs along the branch leading to Coraciimor- the 46 taxa using the MYbaits target enrichment sys- phae and Passeriformes, both of which are generally diur- tem (MYcroarray, Arbor Biosciences) (Additional fle 2: nal [4, 17]. For Coraciimorphae, two PSGs (CNGB3 and Table S2). Te average number of reads sequenced across SLC24A2) were found. CNGB3 and SLC24A2 are cone- our 46 taxa was 4,716,979.58, the average total base pair expressed and are respectively involved in photoresponse yield was