Distant Drumming: morphological correlates of habitat and courtship behaviour in the Ruffed Grouse (Bonasa umbellus)

The Ruffed Grouse (Bonasa umbellus) is a resident game bird of North America. Unlike other birds, male Ruffed Grouse do not vocalize during courtship, and are dependent upon ‘drumming’, a ‘wingbeat’ display, for the acoustic component of their courtship behaviour. Because this wingbeat display is unique, I investigated morphological correlates that could underlie its production. First, I examined wing shape among grouse from museum specimens using various morphometrics. I found that wing morphology corresponds with habitat, behaviour and phylogentic relationships within Tetraoninae. Next, I examined the brains of male and female Ruffed Grouse. I detected seasonal plasticity between males collected during the breeding and non-breeding seasons; those collected during the breeding season had larger motor regions than those collected during the non-breeding season. My findings indicate that habitat and wing shape are correlated among grouse, and that seasonal changes in brain morphology contribute to the production of the drumming display

Mosaic and Concerted Evolution in the Visual System of Birds

<div><p>Two main models have been proposed to explain how the relative size of neural structures varies through evolution. In the mosaic evolution model, individual brain structures vary in size independently of each other, whereas in the concerted evolution model developmental constraints result in different parts of the brain varying in size in a coordinated manner. Several studies have shown variation of the relative size of individual nuclei in the vertebrate brain, but it is currently not known if nuclei belonging to the same functional pathway vary independently of each other or in a concerted manner. The visual system of birds offers an ideal opportunity to specifically test which of the two models apply to an entire sensory pathway. Here, we examine the relative size of 9 different visual nuclei across 98 species of birds. This includes data on interspecific variation in the cytoarchitecture and relative size of the isthmal nuclei, which has not been previously reported. We also use a combination of statistical analyses, phylogenetically corrected principal component analysis and evolutionary rates of change on the absolute and relative size of the nine nuclei, to test if visual nuclei evolved in a concerted or mosaic manner. Our results strongly indicate a combination of mosaic and concerted evolution (in the relative size of nine nuclei) within the avian visual system. Specifically, the relative size of the isthmal nuclei and parts of the tectofugal pathway covary across species in a concerted fashion, whereas the relative volume of the other visual nuclei measured vary independently of one another, such as that predicted by the mosaic model. Our results suggest the covariation of different neural structures depends not only on the functional connectivity of each nucleus, but also on the diversity of afferents and efferents of each nucleus.</p></div

Location, borders and cytoarchitecture of other visual nuclei.

<p>Photomicrographs of coronal sections showing the location and borders of the different visual nuclei in birds. <b>A</b>, shows the isthmo optic nucleus (<b>ION</b>) in a songbird (Passeriformes) the Spotted Pardalote (<i>Pardalotus punctatus</i>). <b>B</b> shows the nucleus of the basal optic root (<b>nBOR</b>) in an owl (Strigiformes), the Northern Hawk Owl (<i>Surnia ulula</i>). <b>C</b> shows the nucleus lentiformis mesencephali (<b>LM</b>), the ventral part of the geniculate nucleus (<b>GLv</b>) and the nucleus rotundus (nRt) in a Gruiform, the American Coot (<i>Fulica americana</i>). <b>D</b> shows the optic tectum (<b>TeO</b>) in a gallinaceous bird (Galliformes) the Ring-necked Pheasant (<i>Phasianus colchicus</i>).</p

Relative size of nucleus semilunaris.

<p>Scatterplot of log-transformed volume of nucleus semilunaris (<b>SLu</b>) plotted as a function of the log-transformed brain volume minus the SLu volume (<b>A</b>) or the log-transformed volume of the optic tectum (<b>TeO</b>; <b>B</b>) for all species examined (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0090102#pone.0090102.s001" target="_blank">table S1</a>). The bar graph shows the relative size of SLu relative to the brain (<b>B</b>) or the TeO (<b>C</b>). Values shown are the means of the residuals derived from the respective regressions shown in <b>A</b> and <b>C</b>.</p

Relative size of other visual nuclei.

<p>Scatterplot of log-transformed volume of different nuclei plotted as a function of the log-transformed brain volume minus the volume of the respective nuclei (<b>A</b>, <b>C</b>, <b>E</b>, <b>G</b> and <b>I</b>). The bar graphs show the relative size each nucleus relative to the brain, represented as the mean of the residuals derived from the respective regressions (<b>B</b>, <b>D</b>, <b>F</b>, <b>H</b> and <b>K</b>). <b>A–B</b>, Scatterplot and bar graph for the isthmo optic nucleus (<b>ION</b>). <b>C–D</b>, Scatterplot and bar graph for the ventral geniculate nucleus (<b>GLv</b>). The white triangles indicate gallinaceous birds and black circles to all other birds studied. <b>E–F</b>, Scatterplot and bar graph for the nucleus of the basal optic root (<b>nBOR</b>). <b>G–H</b>, Scatterplot and bar graph for the nucleus lentiformis mesencephali (<b>LM</b>). The white triangles indicate gallinaceous birds, the open circles indicate hummingbirds and the black circles are all other birds species studied.</p

Visual nuclei bivariate allometric coefficients.

<p>Coefficients of the bivariate allometric relationship between visual nuclei calculated from the loading of each nucleus in the first principal component of a phylogenetically corrected PCA performed with Hacket et al., (2008; <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0090102#pone.0090102-Hackett1" target="_blank">[68]</a>) phylogeny (see Methods for calculations details).</p

Location, borders and cytoarchitecture of the isthmal complex.

<p>Photomicrographs showing the location and borders of the three isthmal nuclei, the magnocellular and parvocellular portions of nucleus isthmi (<b>Imc</b>, <b>Ipc</b>) and the nucleus semilunaris (<b>SLu</b>) in four species of birds. <b>A</b>–<b>C</b> show the isthmal complex in the three different groups of birds that exhibited a Imc segregated in two layers, the internal subdivision of the Imc (Imc-in) and the external subdivision of the Imc (Imc-ex). <b>A</b> shows a songbird (Passeriformes), the Gouldian Finch (<i>Erythrura gouldiae</i>). <b>B</b> shows a Gruiform, the American Coot (<i>Fulica Americana</i>). <b>C</b> shows a woodpecker (Piciformes), the Yellow-bellied Sapsucker (<i>Sphyrapicus varius</i>); <b>D</b> shows a pigeon (Columbiformes), the Bar-shouldered Dove (<i>Geopelia humeralis</i>). <b>E</b> and <b>F</b> show two species of owls (Strigiformes), the Short-eared Owl (<i>Asio flammeus</i>) and the Northern Hawk Owl (<i>Surnia ulula</i>).</p

Tissue quality examples.

<p>Photomicrographs of Nissl stained coronal sections in four of the specimens used in this study. <b>A</b> and <b>C</b> show two of the lowest quality staining used in this study while <b>B</b> and <b>D</b> show sections equivalent to the ones showed in A and C in specimens with good quality of staining, Notice that even in <b>A</b> and <b>C</b>, the borders of visual structures measured in this study, like the nucleus lentiformis mecencephali (<b>LM</b>), the ventral part of the geniculate nucleus (<b>GLv</b>), the nucleus rotundus (<b>nRt</b>), the nucleus of the basal optic root (<b>nBOR</b>) and the optic tectum (<b>TeO</b>), are all clearly discernible. In <b>A</b>, the white arrows show the borders between LM and the nucleus laminaris precommissuralis (<b>LPC</b>) and also the dorsal border of GLv. In <b>C</b>, the white arrows show the border of nBOR. Scales bars = 400 µm.</p

Results of principal component analysis.

<p>Loadings, eigenvalues and cumulative amount of variation explained by four of the components (PC's) obtained from a PCA analysis using the log-transformed volume or the relative size (residuals, see methods) of nine visual nuclei. Values obtained using Hackett et al., (2008; <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0090102#pone.0090102-Hackett1" target="_blank">[68]</a>) phylogeny are shown. Values obtained with two different evolutionary models (Brownian motion and pagel's lambda) are also shown for the relative size PCA. For complete values with both phylogenies used in this study see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0090102#pone.0090102.s005" target="_blank">table S5</a>.</p