Vasotocin and the evolution of avian sociality

Make Him a Monogamy Junkie

The Monogamy Method

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In addition to differing in mating system, the monogamous and non-monogamous rodents discussed above diverge in other aspects of social organization. For example, the monogamous vole species often form small groups and exhibit biparental care (Getz et al., 2005), whereas the non-monogamous species typically do not. Given that the nonapeptides are relevant for the regulation of various affiliative and paternal behaviours in addition to pair bonding (Wang et al., 1994; Parker and Lee, 2001; Bales et al., 2004), the question arises as to whether peptidergic mechanisms evolve specifically in relation to a given aspect of social organization (such as mating system, parental care, or sociality) or whether multiple dimensions of behaviour are obligatorily linked together in relation to nonapeptide function. However, rodents do not offer good opportunities to address these questions, since the various aspects of behaviour cannot be adequately uncoupled in comparative studies of different species (for discussion, see Goodson et al., 2006).

In contrast to rodents, however, some bird groups offer excellent opportunities to isolate various aspects of social organization as quasi-independent variables. Finches and waxbills of the family Estrildidae are particularly useful in this regard, since sociality (i.e. grouping behaviour) can be isolated from other aspects of behaviour and ecology. The estrildids are all monogamous (forming long-term or life-long pair bonds) and exhibit biparental care. Most of the species are moderately social — flocking during the non-breeding season and loosely distributing for breeding. However, some species have evolved to be gregarious year-round and a few species have evolved highly colonial breeding. At the other end of the continuum, a small number of estrildid species live year-round as relatively asocial malefemale pairs and aggressively defend territories (Skead, 1975; Goodwin, 1982). Our studies have included five species of estrildids, including two territorial species that likely evolved territoriality independently; two highly gregarious species that independently evolved coloniality; and an intermediate, modestly gregarious species (Goodson et al., 2005, 2006; Goodson and Wang, 2006).

Our primary research focus in these birds has been on the response characteristics of the AVT neurons in the BSTm. AVT/AVP cells of the BSTm likely contribute to the regulation of multiple affiliative behaviours, including pair bonding in rodents (Young and Wang, 2004; De Vries and Panzica, 2006), but no research had previously determined how different classes of social stimuli elicit responses in these neurons. To address this issue, we used double-label immuno-cytochemistry to examine the induction of Fos (a marker of neuronal activity) in AVT-ir neurons following a control manipulation or exposure to a same-sex conspecific through a wire barrier (both sexes were examined, although no sex differences were observed). A significant interaction effect was obtained (species x condition), reflecting the fact that in the territorial species, exposure to a samesex conspecific tended to decrease the colocaliza-tion of immunoreactive AVT and Fos, whereas colocalization tended to increase in the highly gregarious species. The modestly gregarious species exhibited virtually no change in the colocali-zation of AVT and Fos (Goodson and Wang, 2006). Importantly, the testing paradigm that we employed limits the overt expression of social behaviours; thus, the species differences in Fos response should primarily reflect differences in perceptual or motivational processes, not differences in behavioural response.

The data just described suggest the hypothesis that BSTm AVT neurons may exhibit increases in Fos expression following exposure to "positive" stimuli that normally elicit affiliative responses, but not to "negative" stimuli that normally elicit aggression or aversion. Such a valence sensitivity could readily account for divergent responses to same-sex stimuli in territorial and gregarious species. Two additional findings firmly support our hypothesis. First, in the territorial violet-eared waxbill (Uraeginthus granatina), exposure to a same-sex conspecific produces a significant decrease in AVT-Fos colocalization, whereas exposure to a positive social stimulus, the subject's pair bond partner, produces a very robust increase (Fig. 2A). Similarly, in the highly gregarious zebra finch (Taeniopygia guttata), significant increases in AVT-Fos colocalization are observed in a mate competition paradigm if the subjects are allowed to court, but not if the subjects are aggressively subjugated (Fig. 2B; Goodson and Wang, 2006). Recent findings from our laboratory further demonstrate that the AVT-ir neurons of the BSTm are sensitive only to positive social stimuli, since positive non-social stimuli are without effect (Goodson, unpublished observations).

Consistent with these findings, we found that: (1) the two highly gregarious, colonially breeding species have significantly more AVT-ir neurons in the BSTm than do the other species, (2) the territorial species have lower baseline levels of AVT-Fos colocalization than do the gregarious species and (3) the three gregarious species have

  1. 2. AVT neuronal responses to social stimuli (adapted with permission from Goodson and Wang, 2006). (A) Percentage of AVT-ir neurons in the BSTm that express Fos-ir nuclei (means+ SEM) in the relatively asocial violet-eared waxbill following exposure to a control condition (open bars), a samesex conspecific (black bars) or the subject's pair bond partner (grey bars). Different letters above the bars indicate significant group differences (Mann-Whitney tied p<0.05, following significant Kruskal-Wallis tied p = 0.003). Total n = 16. (B) AVT + Fos colocalization in control (open bars), subjugated (black bars) and non-subjugated (grey bars) zebra finches exposed to mate competition (Kruskal-Wallis tied p = 0.03). No sex differences were observed and sexes are shown pooled. Total n 15.
  2. 2. AVT neuronal responses to social stimuli (adapted with permission from Goodson and Wang, 2006). (A) Percentage of AVT-ir neurons in the BSTm that express Fos-ir nuclei (means+ SEM) in the relatively asocial violet-eared waxbill following exposure to a control condition (open bars), a samesex conspecific (black bars) or the subject's pair bond partner (grey bars). Different letters above the bars indicate significant group differences (Mann-Whitney tied p<0.05, following significant Kruskal-Wallis tied p = 0.003). Total n = 16. (B) AVT + Fos colocalization in control (open bars), subjugated (black bars) and non-subjugated (grey bars) zebra finches exposed to mate competition (Kruskal-Wallis tied p = 0.03). No sex differences were observed and sexes are shown pooled. Total n 15.

significantly higher densities of V1a-like binding sites in the LS than do the territorial species (Fig. 3) (Goodson and Wang, 2006; Goodson et al., 2006). In rodents, septal V1a receptors promote active social interaction and facilitate social recognition (Landgraf et al., 2003) - functions that should be in higher demand for gregarious species than for territorial species.

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