Nasonia Parasitic Wasps Escape from Haller's Rule by Diphasic, Partially Isometric Brain-Body Size Scaling and Selective Neuropil Adaptations.
ABSTRACT: Haller's rule states that brains scale allometrically with body size in all animals, meaning that relative brain size increases with decreasing body size. This rule applies both on inter- and intraspecific comparisons. Only 1 species, the extremely small parasitic wasp Trichogramma evanescens, is known as an exception and shows an isometric brain-body size relation in an intraspecific comparison between differently sized individuals. Here, we investigated if such an isometric brain-body size relationship also occurs in an intraspecific comparison with a slightly larger parasitic wasp, Nasonia vitripennis, a species that may vary 10-fold in body weight upon differences in levels of scramble competition during larval development. We show that Nasonia exhibits diphasic brain-body size scaling: larger wasps scale allometrically, following Haller's rule, whereas the smallest wasps show isometric scaling. Brains of smaller wasps are, therefore, smaller than expected and we hypothesized that this may lead to adaptations in brain architecture. Volumetric analysis of neuropil composition revealed that wasps of different sizes differed in relative volume of multiple neuropils. The optic lobes and mushroom bodies in particular were smaller in the smallest wasps. Furthermore, smaller brains had a relatively smaller total neuropil volume and larger cellular rind than large brains. These changes in relative brain size and brain architecture suggest that the energetic constraints on brain tissue outweigh specific cognitive requirements in small Nasonia wasps.
Project description:Trichogramma evanescens parasitic wasps show large phenotypic plasticity in brain and body size, resulting in a 5-fold difference in brain volume among genetically identical sister wasps. Brain volume scales linearly with body volume in these wasps. This isometric brain scaling forms an exception to Haller's rule, which states that small animals have relatively larger brains than large animals. The large plasticity in brain size may be facilitated by plasticity in neuron size, in the number of neurons, or both. Here, we investigated whether brain isometry requires plasticity in the number and size of monoaminergic neurons that express serotonin (5HT), octopamine (OA), and dopamine (DA). Genetically identical small and large T. evanescens appear to have the same number of 5HT-, OA-, and DA-like immunoreactive cell bodies in their brains, but these cell bodies differ in diameter. This indicates that brain isometry can be facilitated by plasticity in the size of monoaminergic neurons, rather than plasticity in numbers of monoaminergic neurons. Selection pressures on body miniaturization may have resulted in the evolution of miniaturized neural pathways that allow even the smallest wasps to find suitable hosts. Plasticity in the size of neural components may be among the mechanisms that underlie isometric brain scaling while maintaining cognitive abilities in the smallest individuals.
Project description:Heritable genetic variation in relative brain size can underlie the relationship between brain performance and the relative size of the brain. We used bidirectional artificial selection to study the consequences of genetic variation in relative brain size on brain morphology, cognition and longevity in Nasonia vitripennis parasitoid wasps. Our results show a robust change in relative brain size after 26 generations of selection and six generations of relaxation. Total average neuropil volume of the brain was 16% larger in wasps selected for relatively large brains than in wasps selected for relatively small brains, whereas the body length of the large-brained wasps was smaller. Furthermore, the relative volume of the antennal lobes was larger in wasps with relatively large brains. Relative brain size did not influence olfactory memory retention, whereas wasps that were selected for larger relative brain size had a shorter longevity, which was even further reduced after a learning experience. These effects of genetic variation on neuropil composition and memory retention are different from previously described effects of phenotypic plasticity in absolute brain size. In conclusion, having relatively large brains may be costly for N. vitripennis, whereas no cognitive benefits were recorded.
Project description:Body size reduction in mammals is usually associated with only moderate brain size reduction, because the brain and sensory organs complete their growth before the rest of the body during ontogeny. On this basis, 'phyletic dwarfs' are predicted to have a greater relative brain size than 'phyletic giants'. However, this trend has been questioned in the special case of dwarfism of mammals on islands. Here we show that the endocranial capacities of extinct dwarf species of hippopotamus from Madagascar are up to 30% smaller than those of a mainland African ancestor scaled to equivalent body mass. These results show that brain size reduction is much greater than predicted from an intraspecific 'late ontogenetic' model of dwarfism in which brain size scales to body size with an exponent of 0.35. The nature of the proportional change or grade shift observed here indicates that selective pressures on brain size are potentially independent of those on body size. This study demonstrates empirically that it is mechanistically possible for dwarf mammals on islands to evolve significantly smaller brains than would be predicted from a model of dwarfing based on the intraspecific scaling of the mainland ancestor. Our findings challenge current understanding of brain-body allometric relationships in mammals and suggest that the process of dwarfism could in principle explain small brain size, a factor relevant to the interpretation of the small-brained hominin found on the Island of Flores, Indonesia.
Project description:A common allometric pattern called Haller's Rule states that small species have relatively larger brains and eyes than larger species of the same taxonomic group. This pattern imposes drastic structural changes and energetic costs on small species to produce and maintain a disproportionate amount of nervous tissue. Indeed, several studies have shown the significant metabolic costs of having relatively larger brains; however, little is known about the structural constraints and adaptations required for housing these relatively larger brains and eyes. Because hummingbirds include the smallest birds, they are ideal for exploring how small species evolve morphological adaptations for housing relatively larger brain and eyes. We here present results from a comparative study of hummingbirds and show that the smallest species have the lowest levels of ossification, the most compact braincases, and relatively larger eye sockets, but lower eye/head proportion, than larger species. In contrast to Passerines, skull ossification in hummingbirds correlates with body and brain size but not with age. Correlation of these skull traits with body size might represent adaptations to facilitate housing relatively larger brain and eyes, rather than just heterochronic effects related to change in body size. These structural changes in skull traits allow small animals to accommodate disproportionately larger brains and eyes without further increasing overall head size.
Project description:Understanding intraspecific geographic variation in animal signals poses a challenging evolutionary problem. Studies addressing geographic variation typically focus on signals used in mate-choice, however, geographic variation in intrasexual signals involved in competition is also known to occur. In Polistes dominulus paper wasps, females have black facial spots that signal dominance: individuals wasps with more complex 'broken' facial patterns are better fighters and are avoided by rivals. Recent work suggests there is dramatic geographic variation in these visual signals of quality, though this variation has not been explicitly described or quantified. Here, we analyze variation in P. dominulus signals across six populations and explore how environmental conditions may account for this variation. Overall, we found substantial variation in facial pattern brokenness across populations and castes. Workers have less broken facial patterns than gynes and queens, which have similar facial patterns. Strepsipteran parasitism, body size and temperature are all correlated with the facial pattern variation, suggesting that developmental plasticity likely plays a key role in this variation. First, the extent of parasitism varies across populations and parasitized individuals have lower facial pattern brokenness than unparasitized individuals. Second, there is substantial variation in body size across populations and a weak but significant relationship between facial pattern brokenness and body size. Wasps from populations with smaller body size (e.g. Italy) tend to have less broken facial patterns than wasps from populations with larger body size (e.g. New York, USA). Third, there is an apparent association between facial patterns and climate, with wasp from cooler locations tending to have higher facial pattern brokenness than wasps from warmer locations. Additional experimental work testing the causes and consequences of facial pattern variation will be important, as geographic variation in signals has important consequences for the evolution of communication systems and social behavior.
Project description:BACKGROUND: Most evolutionary studies on the size of brains and different parts of the brain have relied on interspecific comparisons, and have uncovered correlations between brain architecture and various ecological, behavioural and life-history traits. Yet, similar intraspecific studies are rare, despite the fact that they could better determine how selection and phenotypic plasticity influence brain architecture. We investigated the variation in brain size and structure in wild-caught nine-spined sticklebacks (Pungitius pungitius) from eight populations, representing marine, lake, and pond habitats, and compared them to data from a previous common garden study from a smaller number of populations. RESULTS: Brain size scaled hypo-allometrically with body size, irrespective of population origin, with a common slope of 0.5. Both absolute and relative brain size, as well as relative telencephalon, optic tectum and cerebellum size, differed significantly among the populations. Further, absolute and relative brain sizes were larger in pond than in marine populations, while the telencephalon tended to be larger in marine than in pond populations. These findings are partly incongruent with previous common garden results. A direct comparison between wild and common garden fish from the same populations revealed a habitat-specific effect: pond fish had relatively smaller brains in a controlled environment than in the wild, while marine fish were similar. All brain parts were smaller in the laboratory than in the wild, irrespective of population origin. CONCLUSION: Our results indicate that variation among populations is large, both in terms of brain size and in the size of separate brain parts in wild nine-spined sticklebacks. However, the incongruence between the wild and common garden patterns suggests that much of the population variation found in the wild may be attributable to environmentally induced phenotypic plasticity. Given that the brain is among the most plastic organs in general, the results emphasize the view that common garden data are required to draw firm evolutionary conclusions from patterns of brain size variability in the wild.
Project description:Primates are usually found to have richer behavioral repertoires and better cognitive abilities than rodents of similar brain size. This finding raises the possibility that primate brains differ from rodent brains in their cellular composition. Here we examine the cellular scaling rules for primate brains and show that brain size increases approximately isometrically as a function of cell numbers, such that an 11x larger brain is built with 10x more neurons and approximately 12x more nonneuronal cells of relatively constant average size. This isometric function is in contrast to rodent brains, which increase faster in size than in numbers of neurons. As a consequence of the linear cellular scaling rules, primate brains have a larger number of neurons than rodent brains of similar size, presumably endowing them with greater computational power and cognitive abilities.
Project description:Chalcidoid wasps represent one of the most speciose superfamilies of animals known, with ca. 23,000 species described of which many are parasitoids. They are extremely diverse in body size, morphology and, among the parasitoids, insect hosts. Parasitic chalcidoids utilise a range of behavioural adaptations to facilitate exploitation of their diverse insect hosts, but how host use might influence the evolution of body size and morphology is not known in this group. We used a phylogenetic comparative analysis of 126 chalcidoid species to examine whether body size and antennal size showed evolutionary correlations with aspects of host use, including host breadth (specificity), host identity (orders of insects parasitized) and number of plant associates. Both morphological features and identity of exploited host orders show strong phylogenetic signal, but host breadth does not. Larger body size in these wasps was weakly associated with few plant genera, and with more specialised host use, and chalcidoid wasps that parasitize coleopteran hosts tend to be larger. Intriguingly, chalcidoid wasps that parasitize hemipteran hosts are both smaller in size in the case of those parasitizing the suborder Sternorrhyncha and have relatively larger antennae, particularly in those that parasitize other hemipteran suborders. These results suggest there are adaptations in chalcidoid wasps that are specifically associated with host detection and exploitation.
Project description:Despite important recent progress in our understanding of brain evolution, controversy remains regarding the evolutionary forces that have driven its enormous diversification in size. Here, we report that in passerine birds, migratory species tend to have brains that are substantially smaller (relative to body size) than those of resident species, confirming and generalizing previous studies. Phylogenetic reconstructions based on Bayesian Markov chain methods suggest an evolutionary scenario in which some large brained tropical passerines that invaded more seasonal regions evolved migratory behavior and migration itself selected for smaller brain size. Selection for smaller brains in migratory birds may arise from the energetic and developmental costs associated with a highly mobile life cycle, a possibility that is supported by a path analysis. Nevertheless, an important fraction (over 68%) of the correlation between brain mass and migratory distance comes from a direct effect of migration on brain size, perhaps reflecting costs associated with cognitive functions that have become less necessary in migratory species. Overall, our results highlight the importance of retrospective analyses in identifying selective pressures that have shaped brain evolution, and indicate that when it comes to the brain, larger is not always better.
Project description:Parasitoid wasps are abundant and diverse hymenopteran insects that lay their eggs into the internal body (endoparasitoid) or on the external surface (ectoparasitoid) of their hosts. To make a more conducive environment for the wasps' young, both ecto- and endoparasitoids inject venoms into the host to modulate host immunity, metabolism and development. Endoparasitoids have evolved from ectoparasitoids independently in different hymenopteran lineages. Pteromalus puparum, a pupal endoparasitoid of various butterflies, represents a relatively recent evolution of endoparasitism within pteromalids. Using a combination of transcriptomic and proteomic approaches, we have identified 70 putative venom proteins in P. puparum. Most of them show higher similarity to venom proteins from the related ectoparasitoid Nasonia vitripennis than from other more distantly related endoparasitoids. In addition, 13 venom proteins are similar to venoms of distantly related endoparasitoids but have no detectable venom matches in Nasonia. These venom proteins may have a role in adaptation to endoparasitism. Overall, these results lay the groundwork for more detailed studies of venom function and adaptation to the endoparasitic lifestyle.