Contrasting migratory journeys and changes in hippocampal astrocyte morphology in shorebirds

Abstract

Semipalmated sandpiper (Calidris pusilla) migration to the Southern Hemisphere includes a 5-day non-stop flight over the Atlantic Ocean, whereas semipalmated plover (Charadrius semipalmatus) migration, to the same area, is largely over land, with stopovers for feeding and rest. We compared the number and 3D morphology of hippocampal astrocytes of Ch. semipalmatus before and after autumnal migration with those of C. pusilla to test the hypothesis that the contrasting migratory flights of these species could differentially shape hippocampal astrocyte number and morphology.We captured individuals from both species in the Bay of Fundy (Canada) and in the coastal region of Bragança (Brazil) and processed their brains for selective GFAP immunolabeling of astrocytes. Hierarchical cluster analysis of astrocyte morphological features distinguished two families of morphological phenotypes, named type I and type II, which were differentially affected after migratory flights. Stereological counts of hippocampal astrocytes demonstrated that the number of astrocytes decreased significantly in C. pusilla, but did not change in Ch. semipalmatus. In addition, C. pusilla and Ch. semipalmatus hippocampal astrocyte morphological features were differentially affected after autumnal migration. We evaluated whether astrocyte morphometric variables were influenced by phylogenetic differences between C. pusilla and Ch. semipalmatus, using phylogenetically independent contrast approach, and phylogenetic trees generated by nuclear and mitochondrial markers. Our findings

Shorebird’s Longer Migratory Distances are Associated with Larger ADCYAP1 Microsatellites and Greater Morphological Complexity of Hippocampal Astrocytes

“…The comparison of types I and II of C. semipalmatus with the corresponding morphotypes of C. collaris revealed higher mean values of morphological complexity and volume of the convex hull in the migrant and lower and higher mean values in the resident. We suggest that the differences found between migratory and nonmigratory birds' hippocampal astrocyte morphologies might be related to the adaptive response imposed by the contrasting long-distance migratory ights on learning and memory for recognition of olfactory, geomagnetic and visual cues during migration [17,22,23,86]. Indeed, in the present report when comparing migratory species with each other and with the non-migratory species, we found differences in all comparisons that may re ect adaptive responses to migration.…”

“…In previous studies we investigated the in uence of the contrasting autumn migratory ights of C. pusilla and C. semipalmatus on hippocampal astrocyte morphology of birds captured in the Bay of Fundy (Canada) and in the coastal region of Bragança (Brazil). In this comparative analysis we found that long-distance migratory ight shapes the plasticity of hippocampal Type I and Type II astrocyte morphotypes in different ways, and suggested distinct physiological roles for these cells [22,23].…”

“…The matrices were constructed with the combination of all cells of a given group taken pairwise, followed by the weighted calculation of a scalar Euclidean distance between cells using all morphometric variables. [23,24].…”

“…This system was coupled to a microprocessor that controlled the movements of the microscopic stage with the aid of a specialized program (Neurolucida, MBF Bioscience, Williston, VT USA) to store the spatial information (X, Y, Z coordinates) of each digitized point of interest. Three types of cells were identi ed: protoplasmic, brous and radial astrocytes similar to previous descriptions [22][23][24]. In this study, we used only protoplasmic astrocytes.…”

“…Because the hippocampal formation of migratory birds seems to be the center for integration of all navigation systems [14,17], we explored how the contrasting navigation strategies of the semipalmated sandpiper (Calidris pusilla) and the semipalmated plover (Charadrius semipalmatus) during autumn migration are related to hippocampal astroglia morphology [22][23][24] and size of the ADCYAP1 allele. A combination of genetic, developmental, and epigenetic factors de ne life-long adaptive plasticity of astroglia [25] and morphometric studies of its arbors and molecular pro le have revealed that they may change with environmental enrichment [26][27][28] learning and memory [29][30][31].…”