UC Irvine UC Irvine Previously Published Works Title Developmental Modes and Developmental Mechanisms can Channel Brain Evolution Permalink https://escholarship.org/uc/item/6qq0q0r6 Journal Frontiers in Neuroanatomy, 5 ISSN 1662-5129 Authors Charvet, Christine J. Striedter, Georg F. Publication Date 2011-02-08 License https://creativecommons.org/licenses/by/4.0/ 4.0 Peer reviewed eScholarship.org Powered by the California Digital Library University of California REVIEW ARTICLE published: 08 February 2011 NEUROANATOMY doi: 10.3389/fnana.2011.00004 Developmental modes and developmental mechanisms can channel brain evolution Christine J. Charvet1* and Georg F. Striedter1,2 1 Department of Neurobiology and Behavior, Center for the Neurobiology of Learning and Memory, University of California, Irvine, CA, USA 2 Department of Ecology and Evolutionary Biology, University of California, Irvine, CA, USA Edited by: Anseriform birds (ducks and geese) as well as parrots and songbirds have evolved a Fernando Martinez-Garcia, Universidad disproportionately enlarged telencephalon compared with many other birds. However, parrots de Valencia, Spain and songbirds differ from anseriform birds in their mode of development. Whereas ducks and Reviewed by: Ann B. Butler, George Mason geese are precocial (e.g., hatchlings feed on their own), parrots and songbirds are altricial (e.g., University, USA hatchlings are fed by their parents). We here consider how developmental modes may limit and John Kirn, Wesleyan University, USA facilitate specific changes in the mechanisms of brain development. We suggest that altriciality *Correspondence: facilitates the evolution of telencephalic expansion by delaying telencephalic neurogenesis. We Christine J. Charvet, Department of further hypothesize that delays in telencephalic neurogenesis generate delays in telencephalic Psychology, Cornell University, 229 Uris Hall, Ithaca, NY 14853-7601, USA. maturation, which in turn foster neural adaptations that facilitate learning. Specifically, we e-mail: [email protected] propose that delaying telencephalic neurogenesis was a prerequisite for the evolution of neural circuits that allow parrots and songbirds to produce learned vocalizations. Overall, we argue that developmental modes have influenced how some lineages of birds increased the size of their telencephalon and that this, in turn, has influenced subsequent changes in brain circuits and behavior. Keywords: bird, mode, development, proliferation, evolution INTRODUCTION birds: once in the lineage leading to anseriform birds and at least Parrots, songbirds, and anseriform birds (ducks and geese) have once in the group that gave rise to parrots and songbirds. In this evolved a disproportionately large telencephalon compared with review we show that distinct developmental mechanisms under- many other birds (Figure 1; Portmann, 1947a; Boire and Baron, lie these two independent evolutionary changes in telencephalon 1994; Iwaniuk and Hurd, 2005). Although the proportional size size. We next examine how ancestral developmental modes may of the telencephalon in ducks and geese rivals that in parrots and have influenced changes in developmental mechanisms, which in songbirds, the latter taxa differ from ducks and geese in numerous turn influenced evolutionary changes in behavioral flexibility and respects. First, parrots and songbirds are altricial (their hatchlings learning capacity. are fed by their parents), whereas ducks and geese are precocial (their hatchlings feed on their own; Starck and Ricklefs, 1998). ALTRICIALITY IS A PRE-ADAPTATION FOR DELAYED BRAIN Second, parrots and songbirds enlarge their telencephalon by MATURATION delaying telencephalic neurogenesis (Striedter and Charvet, 2008; Most land birds (e.g., parrots, songbirds, suboscines, owls, Charvet and Striedter, 2009a), whereas ducks and geese enlarge kingfishers, falcons) are altricial (Figure 2; Starck and Ricklefs, their telencephalon before telencephalic neurogenesis begins 1998). That is, their hatchlings are relatively immobile and receive (Charvet and Striedter, 2009b). Finally, parrots and songbirds extensive post-hatching parental care. However, the degree of have evolved a set of telencephalic nuclei responsible for vocal helplessness at hatching varies among land birds (Starck and learning (Nottebohm, 1972; Nottebohm et al., 1976; Doupe and Ricklefs, 1998). For instance, falcons and owls are considered Kuhl, 1999), whereas anseriform birds have evolved an expanded semi-altricial in that their hatchlings are covered with down. trigeminal system that is related to feeding (Dubbeldam and Parrots, songbirds, and suboscines are among the most altricial Visser, 1987; Gutiérrez-Ibáñez et al., 2009). Thus, anseriform birds avian species (Starck and Ricklefs, 1998; Londoño, 2003; Greeny differ form parrots and songbirds in their developmental modes, et al., 2004, 2005). Their hatchlings are naked, have their eyes in brain development, in brain anatomy, and in behavior. closed, and are fed for several weeks after hatching. In general, Recent analyses of avian phylogenetic relationships indicate that the most salient difference between altricial and precocial spe- parrots are the sister group of passerines, which include songbirds cies is that parents feed altricial hatchlings whereas precocial and suboscines (manakins, antbirds, tyrant-flycatchers; Ericson hatchlings feed on their own. et al., 2006; Hackett et al., 2008). Anseriform birds are the sister Altricial and precocial species also differ in the timing of brain group of galliform birds (e.g., chickens), which are distantly related maturation. Specifically, altricial species delay some aspects of to songbirds and parrots (Ericson et al., 2006; Hackett et al., 2008). brain maturation into the post-hatching period relative to pre- Therefore, it is most parsimonious to conclude that the expansion cocial species. This is most evident from the observation that of the telencephalon evolved at least twice independently among altricial (including semi-altricial) species such as parrots, songbirds, Frontiers in Neuroanatomy www.frontiersin.org February 2011 | Volume 5 | Article 4 | 1 Charvet and Striedter Development and brain diversity 4 10 9 8 7 6 3 5 ) 4 3 olume (mm V 2 3 elencephalon 10 T 9 Parrots 8 Songbirds 7 Anseriform birds 6 Galliform birds 5 Other birds 9 2 3 4 5 6 7 8 9 3 4 10 3 10 Brain Volume (mm ) FIGURE 1 | A plot of telencephalon volume versus overall brain volume shows that the telencephalon is disproportionately large in parrots, songbirds (i.e., oscine passerines), and anseriform birds (ducks and geese) compared with galliform birds and diverse other avian species. The other avian species in this graph include mainly pigeons, shorebirds and falcons. Data are from Iwaniuk and Hurd (2005). owls, and pigeons generally exhibit more post-hatching brain growth than precocial species (Figure 3). Given this delayed brain icial growth, we can infer that late-born brain regions, such as the Altr Precocial Altricial - Altricial ecocial telencephalon, are functionally immature at hatching in altricial Pr Semi Semi-Altricial species (Portmann, 1947b; Finlay and Darlington, 1995; Ling et al., shers 1997; Finlay et al., 1998; Striedter and Charvet, 2008). This delayed wls alcons O F Alligators Emus Chickens Ducks King Seriemas SongbirdsSuboscinesParrots brain maturation presumably renders altricial hatchlings relatively helpless and dependent on their parents. Parrots and songbirds exhibit even more post-hatching brain growth than other altricial species (e.g., pigeons, owls; Figure 3; Portmann, 1947b; Starck and Ricklefs, 1998). Most of the post- Land Birds hatching brain growth in parrots and songbirds is due to a late expansion of the telencephalon, which is associated with a gen- eral delay and extension of telencephalic neurogenesis (Striedter and Charvet, 2008; Charvet and Striedter, 2009a). Post-hatching Archosaurs neurogenesis has only been examined in a few parrots (parakeets) and songbirds (canaries, chickadees, zebra finches; Paton and FIGURE 2 | Phylogeny of archosaurs (alligators and birds) shows their Nottebohm, 1984; Kirn and DeVoogd, 1989; Barnea and Nottebohm, modes of development. Parrots, songbirds, suboscines (manakins, antbirds, 1994). Previous work shows that the telencephalon in parakeets tyrant-flycatchers), and kingfishers are altricial, whereas falcons and owls are (Melopsittacus undulatus) and zebra finches (Taeniopygia guttata) semi-altricial. Because most land birds (e.g., suboscines and falcons) are harbors an expanded pool of precursor cells, which persists well into either altricial or semi-altricial, the ancestors of parrots and songbirds were the post-hatching period (Charvet and Striedter, 2008; Striedter and probably either altricial or semi-altricial. This, in turn, implies that the expansion of the telencephalon in parrots and songbirds evolved in a lineage Charvet, 2009). In zebra finches, the major period of telencephalic that was at least semi-altricial. In contrast, many reptiles (e.g., alligators), neurogenesis ends approximately 1 week after hatching, although a paleognaths (e.g., emus), and basal lineages of Neoaves (e.g., galliform and limited amount of telencephalic neurogenesis persists into adult- anseriform birds) are precocial. Thus, ducks and geese were probably hood (DeWulf and Bottjer, 2005; Charvet and Striedter, 2009a; Kirn, precocial when they expanded their telencephalon. The phylogeny is based 2010). In parakeets, the major period of