Sex and seasonal differences in hippocampal volume and neurogenesis in brood‐parasitic brown‐headed cowbirds (Molothrus ater)

Abstract

Brown-headed cowbirds (Molothrus ater) are one of few species in which females show more complex space use than males. Female cowbirds search for, revisit, and parasitize host nests and, in a previous study, outperformed males on an open field spatial search task. Previous research reported a female-biased sex difference in the volume of the hippocampus, a region of the brain involved in spatial memory. Neurons produced by adult neurogenesis may be involved in the formation of new memories and replace older neurons that could cause interference in memory. We tested for sex and seasonal differences in hippocampal volume and neurogenesis of brood-parasitic brown-headed cowbirds and the closely related non-brood-parasitic red-winged blackbird (Agelaius phoeniceus) to determine whether there were differences in the hippocampus that reflected space use in the wild. Females had a larger hippocampus than males in both species, but hippocampal neurogenesis, measured by doublecortin immunoreactivity (DCX+), was greater in female than in male cowbirds in the absence of any sex difference in blackbirds, supporting the hypothesis of hippocampal specialization in female cowbirds. Cowbirds of both sexes had a larger hippocampus with greater hippocampal DCX+ than blackbirds. Hippocampus volume remained stable between breeding conditions, but DCX+ was greater post-breeding, indicating that old memories may be lost through hippocampal reorganization following breeding. Our results support, in part, the hypothesis that the hippocampus of cowbirds is specialized for brood parasitism. © 2016 Wiley Periodicals, Inc. Develop Neurobiol 76: 1275-1290, 2016.

Region-specific neuron recruitment in the hippocampus of brown-headed cowbirdsMolothrus ater(Passeriformes: Icteridae)

“…While the present study does not systematically investigate each possible alternative mechanism or the function of newly recruited neurons, the results demonstrate that topographical differences in sex-dependent neurogenesis may contribute to key neural modification that enhances fitness in cowbirds. This is similar to results reported by Guigueno et al (2016a), who found sex-dependent DCX+ in the Hp of cowbirds whereas no sex difference was demonstrated in a non-parasitic relative. The study presented here reveals that this sex-dependent difference is primarily within the rostral subdivision of the Hp of cowbirds.…”

“…Furthermore, while both round and fusiform DCX cell types were detected in the cowbird brain, the round cells dominated in the Hp sub-regions. A similar pattern was reported by Guigueno et al (2016a) who also found very few fusiform cells in the hippocampus of cowbirds. Therefore, the results presented here do not distinguish between various cell morphologies.…”

“…Even though this was a food finding task rather than a nest searching task, it does imply that the female has superior spatial memory relative to the male. Likewise, it has also been demonstrated that this increased demand for spatial ability is reflected in Hp volume and neuron recruitment, as female cowbirds have a larger Hp volume and more neurogenesis in comparison to males as well as closely related Icterid species that are not brood parasites (Sherry et al 1993;Guigueno et al 2016a). Overall, studies in the cowbird are consistent with the adaptive specialization hypothesis (ASH), which posits that selection can modify behavior as well as the underlying neural mechanisms if such modifications result in enhanced fitness (Krebs 1990).…”

The Avian Hippocampal Formation and the Stress Response

“…However, other species, in different conditions, have different rostrocaudal patterns of neurogenesis. In zebra finches, more new neurons can be found in the caudal than in the rostral parts of the HF [Barnea et al, 2006], and in brown-headed cowbirds and red-winged blackbirds ( Agelaius phoeniceus ) the caudal ventral HF also has a higher density of DCX staining and more DCX+ round and fusiform cells, although the effect is not there in DM area (analysis of the supplementary raw data of Guigueno et al [2016]). The reason for these species differences remain to be investigated.…”

Sex‐specific responses in neuroanatomy of hatchling American kestrels in response to embryonic exposure to the flame retardants bis(2‐ethylhexyl)‐2,3,4,5‐tetrabromophthalate and 2‐ethylhexyl‐2,3,4,5‐tetrabromobenzoate

“…Zoomed-in images of the hippocampus were captured with a Â2.5 objective on a Zeiss Imager M2 light microscope equipped with an AxioCam HRc digital camera (Carl Zeiss) connected to a computer with Zen 2 (Blue Edition [2012]; Carl Zeiss) image analysis software. The boundary between hippocampus and the lateral boundary with the hyperpallium apicale was determined by identifying changes in cell size, density, and alignment, a boundary that resembles that of songbirds ( Figure 1; Guigueno et al 2016). The perimeters of the telencephalon from every second collected section (every 10th total section) and of the hippocampus from every collected section (every fifth total section) were traced in ImageJ (Schneider et al 2012) to measure cross-sectional surface areas.…”