Neurogenomic mechanisms of aggression in songbirds

Abstract

Our understanding of the biological basis of aggression in all vertebrates, including humans, has been built largely upon discoveries first made in birds. A voluminous literature now indicates that hormonal mechanisms are shared between humans and a number of avian species. Research on genetics mechanisms in birds has lagged behind the more typical laboratory species because the necessary tools have been lacking until recently. Over the past 30 years, three major technical advances have propelled forward our understanding of the hormonal, neural, and genetic bases of aggression in birds: (1) the development of assays to measure plasma levels of hormones in free-living individuals, or "field endocrinology"; (2) the immunohistochemical labeling of immediate early gene products to map neural responses to social stimuli; and (3) the sequencing of the zebra finch genome, which makes available a tremendous set of genomic tools for studying gene sequences, expression, and chromosomal structure in species for which we already have large datasets on aggressive behavior. This combination of hormonal, neuroendocrine, and genetic tools has established songbirds as powerful models for understanding the neural basis and evolution of aggression in vertebrates. In this chapter, we discuss the contributions of field endocrinology toward a theoretical framework linking aggression with sex steroids, explore evidence that the neural substrates of aggression are conserved across vertebrate species, and describe a promising new songbird model for studying the molecular genetic mechanisms underlying aggression.

Figure 5.1

Plasma testosterone (T) profiles over the breeding season in males of three passerine species. (A) In song sparrows, T peaks during territory establishment (prebreeding) and again during laying of the first clutch when females are receptive (sexual), and then falls during incubation and feeding (parental). (B) In house sparrows, T peaks during periods of intense competition for nest sites, prior to each of multiple broods. (C) In red-winged blackbirds (Agelaius phoeniceus), males provide little parental care and spend more time on territorial defense; T remains relatively high until the end of the breeding season. Redrawn from data in Wingfield (1984a) and Hegner and Wingfield (1986).

Figure 5.2

(A–E) Correlations between aggressive behavior and Fos-immunoreactive (-ir) cell counts in the subpallial (ventral, ventrolateral) and pallial (dorsal) zones of the caudal lateral septum (LSc.v, LSc.vl, and LSc.d; A–C, respectively), paraventricular hypothalamus (PVN; D), and anterior hypothalamus (AH; E) of male song sparrows exposed to STI (n = 16). The intruder’s cage and a speaker broadcasting song were placed adjacent to the subject’s cage. Subjects showed selective flights to the cage wall adjoining the intruder, providing a good measure of aggressive response. Data are shown as the natural log (ln) of the number of contacts with the wire barrier during a 10-min test. (F–I) Correlations between barrier contacts and Zenk-ir cell counts in the rostral LS (LSr; F), LS.vl (G), lateral zone of the LSc (LSc.l; H), and PVN (I). Cell counts are shown as the number of immunoreactive nuclei per 100 μm². Modified from Goodson et al. (2005b).

Figure 5.3

The percentage of arginine vasotocin (VT) neurons in the PVN that express Fos after a 10-min STI is negatively correlated with aggression (ln, the number of contacts with the cage wall adjoining the intruder’s cage; see Fig. 5.2 caption; n = 16) in song sparrows. Modified from Goodson and Kabelik (2009).

Figure 5.4

(A) Peripheral injections of a novel V1a antagonist that crosses the blood–brain barrier have no effect on resident–intruder aggression in male violet-eared waxbills that are aggressive and typically dominant, but aggression in the context of mate competition is significantly reduced by the antagonist in the same males (B). (C) In males that are typically subordinate, resident–intruder aggression is disinhibited by the same treatments. Modified from Goodson et al. (2009b).

Figure 5.5

Plumage polymorphism in white-throated sparrows. (A) Individuals of the white-stripe (WS) morph have alternating black and white stripes on the crown, bright yellow lores, and a clear white throat patch. (B) Individuals of the tan-stripe (TS) morph have alternating brown and tan stripes on the crown, duller yellow lores, and dark bars within the white throat patch. Photos by Allison Reid. Reprinted from Maney (2008).

Figure 5.6

Medians, IQR, and ranges for (A) aggression scores (number of aggressive acts initiated per hour) and (B) individual ranks (as percent opponents dominated) within social groups. Males were introduced in single-sex groups of six birds (three WS and three TS per group) in indoor aviaries. Aggression scores and ranks were determined 10–14 days later by observing interactions and constructing dominance matrices. During spring-like day lengths (16L:8D), WS males were (A) more aggressive and (B) outranked TS males. Rank was unrelated to morph on short days (8L:16D). The long- and short-day experiments were conducted on different individuals. Data from Horton and Maney, unpublished.

Figure 5.7

Model for the ZAL2^m rearrangement. A minimum of two pericentric inversions, represented by the pairs of dashed lines, are hypothesized to have led to the ZAL2/2^m polymorphism. ZAL2 (top) and ZAL2^m (bottom) are shown along with a hypothetical chromosomal arrangement (middle) that could be either ancestral to both the ZAL2 and ZAL2^m or an intermediate arrangement. Centromeres are represented by filled circles. Dark and light boxes represent segments originating on the short and long arms of the presumed ancestral chromosome, respectively. Free recombination between the ZAL2 and ZAL2^m is limited to the tip of the short arm (hatched boxes).