FEATURE ARTICLE THE NATURAL HISTORY OF MODEL ORGANISMS Neurogenomic insights into the behavioral and vocal development of the zebra finch Abstract The zebra finch (Taeniopygia guttata) is a socially monogamous and colonial opportunistic breeder with pronounced sexual differences in singing and plumage coloration. Its natural history has led to it becoming a model species for research into sex differences in vocal communication, as well as behavioral, neural and genomic studies of imitative auditory learning. As scientists tap into the genetic and behavioral diversity of both wild and captive lineages, the zebra finch will continue to inform research into culture, learning, and social bonding, as well as adaptability to a changing climate. MARK E HAUBER*, MATTHEW IM LOUDER AND SIMON C GRIFFITH Introduction Due to the pronounced sexual differences in The zebra finch Taeniopygia guttata is the most singing and plumage coloration found in the intensively studied species of bird that is main- zebra finch (Figure 1), earlier research quickly tained in captivity in large numbers despite not focused on when and how males learn to copy being a species bred for its meat or eggs, like and produce a tutor(-like) song (e.g. Eales, 1987; the chicken or the quail (reviewed in Brainard and Doupe, 2002; Figure 2A), and Zann, 1996). It became popular as a pet bird in then eventually on how females learn from their the 19th century because it bred well in captivity, (foster) fathers to prefer particular male vocal and was adopted for scientific study in the third displays (Braaten and Reynolds, 1999; Rie- quarter of the 20th century, initially for research bel, 2000). This allowed for the characterization into sexual behaviors (Morris, 1954; Immel- and testing of the functions of male song and its mann, 1972). Later, the zebra finch was used in female perception in the context of acoustic sex- *For correspondence: studies of the de novo evolution of vocal culture ual dimorphism at the behavioral, endocrine, [email protected] (e.g. Fehe´r et al., 2009; Diez and MacDougall- and neurophysiological levels (reviewed in Rie- Competing interests: The Shackleton, 2020), the neuroethology of imita- bel, 2009; Hauber et al., 2010). authors declare that no tive vocal learning (Terpstra et al., 2004; The zebra finch was the second avian species to have its genome sequenced (Warren et al., competing interests exist. Vallentin et al., 2016; Yanagihara and Yazaki- 2010), after the domestic fowl (Gallus gallus; Funding: See page 12 Sugiyama, 2019), the neural mechanisms of sen- International Chicken Genome Sequencing sorimotor learning (Mandelblat-Cerf et al., Reviewing editor: Helena Pe´rez Consortium, 2004). Soon after the appearance Valle, eLife, United Kingdom 2014; Okubo et al., 2015; Mackevicius et al., of transgenic lines of domestic fowl and the Jap- 2020; Sakata and Yazaki-Sugiyama, 2020), and Copyright Hauber et al. This anese quail Cortunix japonica (reviewed the role of early acoustic experience on the article is distributed under the by Sato and Lansford, 2013), the first genera- terms of the Creative Commons song-based preferences of female mate choice tions of transgenic zebra finches become avail- Attribution License, which (Riebel and Smallegange, 2003; Chen et al., able (e.g. Agate et al., 2009; Abe et al., 2015; permits unrestricted use and 2017; Woolley, 2012; see the following video Liu et al., 2015). The proven feasibility of redistribution provided that the for a mating display in zebra finches: https:// original author and source are genome editing in both developing zebra www.youtube.com/watch?v=TaC6D1cW1Hs). credited. finches (e.g. Ahmadiantehrani and London, Hauber et al. eLife 2021;10:e61849. DOI: https://doi.org/10.7554/eLife.61849 1 of 19 Feature Article The Natural History of Model Organisms: Insights into the behavioral and vocal development of the zebra finch Figure 1. Adult zebra finches in the wild. Four female and nine male adult zebra finches in the wild in Australia. As the species experiences increasingly extreme climatic fluctuations, future field studies of the zebra finch should also advance our understanding how opportunistically breeding species are able to adapt to accelerating climate change (photo credit: Simon C Griffith). 2017) and adult poultry (reviewed in Finally, with Australia experiencing increas- Woodcock et al., 2017), means that this bird ingly extreme climatic events and fluctuations, may also be used as both a basic and an applied field studies of the zebra finch are also paving (i.e., biomedical) model for development and for the way to understanding how this opportunisti- human health and disease (e.g. Han and Park, cally breeding species is adapting to accelerat- 2018; London, 2020). ing climate change. For example, recent wild Studies of zebra finch natural history in Aus- studies have revealed the zebra finch’s extensive tralia have been essential to establish and con- behavioral and physiological plasticity to with- firm the rationale for studying this species as a stand extreme temperatures of over 40˚C (e.g. model for acoustic communication (Zann, 1990; Cooper et al., 2020a; Cooper et al., 2020b; Elie et al., 2010), social behavior Funghi et al., 2019). In turn, studies of captive (McCowan et al., 2015; Brandl et al., 2019a; zebra finches in controlled temperature condi- Brandl et al., 2019b), reproductive physiology tions have already tested the effects of cool vs. (Perfito et al., 2007), life-long pair bonding hot climates on parental investment (Mariette and Griffith, 2012), and adaptations (Nord et al., 2010), parent-offspring embryonic to heat (Cade et al., 1965; Cooper et al., communication (Mariette and Buchanan, 2016), 2020a; Cooper et al., 2020b). Specifically, by offspring development (Wada et al., 2015), understanding the natural history of the zebra tutor choice for song learning (Katsis et al., finch, research in captivity can capitalize on the manipulation of the behavioral, neuroendocrine, 2018), adult phenotype (e.g. body size: and epigenetic bases of the bird’s phenotype, Andrew et al., 2017), the level of DNA methyla- including conspecific brood parasitism, parent- tion (Sheldon et al., 2020), and the effect of offspring conflict, and sibling rivalry. heat waves on sperm (Hurley et al., 2018). Hauber et al. eLife 2021;10:e61849. DOI: https://doi.org/10.7554/eLife.61849 2 of 19 Feature Article The Natural History of Model Organisms: Insights into the behavioral and vocal development of the zebra finch g. song) variability (Lansverk et al., 2019; see Box 1). An evolutionary history of the zebra finch The zebra finch is endemic to Australasia, and evolved there as part of the Australian grass finch radiation within the Estrildidae (Olsson and Alstro¨m, 2020). The species shares a common ancestor with Poephila finches (long-tailed P. acuticauda; black-throated P. cincta; and masked finch P. personata), diverging around 2.9 million years ago (Singhal et al., 2015). For- merly, the zebra finch was placed in a genus with the double-barred finch (Taeniopygia biche- novii), but in fact these two lineages diverged around 3.5 million years ago (Singhal et al., 2015). Two subspecies of the zebra finch are recog- nized, with the continental Australian taxon (T. guttata castanotis) having no clear genetic struc- ture and apparently mating randomly within its breeding population (Balakrishnan and Edwards, 2009). The other subspecies is the Timor zebra finch (T. g. guttata), found to the north of Australia. The genetic divergence between the two lineages suggests that the lat- Figure 2. Timeline and brain pathways of auditory and vocal learning in the zebra finch. (A) ter taxon colonized the Lesser Sunda Islands Timeline of sensory (auditory learning) and sensory-motor (vocal self-assessment and song- around 1 million years ago and has a reduced production) critical periods in zebra finch song development. (B) Brain nuclei of male zebra diversity and genetic distance driven by found- finches for auditory learning (CN: cochlear nucleus; MLd: mesencephalicus lateralis pars ing effects and selection, relative to the conti- dorsalis; OV: nucleus ovoidalis; field L: primary auditory forebrain input area; NCM: nental subspecies (Balakrishnan and Edwards, caudomedial nidopallium; CMM: caudomedial mesopallium; VTA: ventral tegmental area; 2009). The insular subspecies has also been and AIV: ventral portion of the intermediate arcopallium), vocal learning (HVC, Area X: basal ganglia; LMAN: lateral magnocellular nucleus of the anterior nidopallium; DLM: nucleus occasionally studied in captivity, and it differs dorsolateralis anterior thalami, pars medialis), and vocal production (HVC, and RA: robust from the continental Australian subspecies in nucleus of the arcopallium). morphological and behavioral traits, including song rate and mate choice (Clayton, 1990; Clayton et al., 1991). By tapping into the existing genetic and The two subspecies of the zebra finch are behavioral diversity of wild and captive lineages physically isolated from one another in the wild, in zebra finches (e.g. Forstmeier et al., 2007; but they can readily hybridize and be back- Knief et al., 2015) to perform comparative avian crossed in captivity to examine a range of ques- genomic analyses (Jarvis et al., 2014; tions in classical genetics and functional devel- Feng et al., 2020), interspecific hybridization opmental biology. To date, this approach has studies (Woolley and Sakata, 2019; seen limited application, with