Abstract

Extant lampreys represent the earliest vertebrates and are therefore of great interest for the study of brain evolution and the ancestral condition of the vertebrate brain. Additionally, due to their protracted lifestyle, these fishes represent an excellent model for understanding the role ecological factors play in the develop- ment of the brain in a diversity of habitats. However, little is known about the ontogenetic or phylogenetic variability of their nervous system. We investigated the changes in brain size and brain struc- ture size during ontogeny in representatives of all three families of lampreys and were interested to reveal whether there were any dif- ferences in brain organization associated with a stage of the life cycle or additional ecological, with implications for specialization of individual sensory modalities. Body mass and brain mass were obtained from 55 individuals from 17 species at each of the five phases of the life cycle, representing 33 independent data points for ammocoetes or larvae (n = 9), metamorphosing individuals (n = 3), downstream migrants (n = 8), upstream migrants (n = 4) and spawning adults (n = 8). We found that the brain mass in- creased with body mass according to the allometric relationship y = 0.48x + 1.02 (R2 = 0.59, n = 33; slope significance at p = 0.001). Results from an analysis of variance (ANOVA) revealed that body size had a significantly positive effect on brain size (p = 0.001), which was similar across the different life history stages. A post- hoc Tukey analysis showed that ammocoetes had significantly smaller brains than individuals at post-metamorphic stages (p < 0.05), whereas we found no significant differences in brain size between individuals after metamorphosis. Volumes of the olfac- tory bulbs, the telencephalic lobes, the pineal organ, the optic tec- ta, the octavo-trigeminal region (V–VIII nerve), and the gustatory area (IX–XII nerve) were approximated using the idealized half- ellipsoid/ellipsoid method. To account for the phylogenetic relat- edness between species, phylogenetic generalized least-squares (pGLS) models of evolutionary change were also constructed to test for correlates of brain evolution. Akaike’s information criteria (AICs) were used to identify the most parsimonious model, which showed that, for some major brain regions, ecological factors such as habitat, diet, and parasitism exerted a significant influence on brain structure size. Remarkably, the best-fit models for olfactory bulb size included parasitism and diet as factors, which was conse- quently confirmed by an analysis of covariance (ANCOVA), where parasitic species have a higher rate of development of the olfactory bulbs compared to non-parasitic species. Based on our results, we predict that animals at each life history stage experience a wide range of environmental cues within their primary habitat, thus influencing different sensory systems, which may be reflected in changes in brain organization throughout ontogeny. This work offers a unique opportunity to understand how phylogenetic con- straints and environmental signals influence the development of the brain in a basal vertebrate.