Early environmental conditions affect the volume of higher-order brain centers in a jumping spider

P.O.M. Steinhoff, J. Liedtke, A. Sombke, J.M. Schneider & G. Uhl, Journal of ZoologyDOI: 10.1111/jzo.12512

The brain enables animals to vary their behavior in response to environmental conditions. In order to react to changes in the environment, changes in the anatomy of the brain can be advantageous. Changes of the physical or the social environment may pose different challenges to the anatomical setup of the brain. It is often assumed that interactions with conspecifics require higher brain complexity compared to interactions with the physical environment.

That’s where we come in: we investigated whether early environmental conditions have an effect on the brain development of jumping spiders (Marpissa muscosa), and if yes, which factors are most important. To test this, we reared jumping spiders under different physical and social conditions. We wanted to know whether growing up with or without conspecifics and in a complex or simple environment has an effect on the development of the brain in these animals.

Figure 1
Female Marpissa muscosa © Jannis Liedtke

Jumping spiders are extraordinary arthropods that are known for a wide array of complex behaviors, such as elaborate hunting techniques and multimodal courtship displays. They are able to learn and solve complex tasks. They have exceptionally good eyesight – the best among all arthropods, even better than some mammals. From previous studies, it is known that the jumping spider Marpissa muscosa is capable of reversal learning, and that rearing conditions affect their exploration tendency, social behavior and learning ability. Our study published in the Journal of Zoology tackles the question whether these differences in behavior and learning ability are mirrored by differences in brain volumes.

The spiders were reared in one of three environments. In the physically enriched treatment, spiders grew up alone in a plastic box enriched with physical objects, such as bark, moss and strings. In the socially enriched environment, spiders grew up together in groups of up to 15 individuals in a larger but physically not enriched box. Finally, in the deprived environment, spiders grew up alone in boxes that were smaller and physically not enriched.

Figure 2
Female Marpissa muscosa within the physically enriched setting © Philip O.M. Steinhoff

After the spiders reached maturity, we investigated their brains with micro-computed tomography (microCT), and calculated the volumes of different brain areas. MicroCT analysis allows the investigation of internal organs in small animals without the need for dissection and is thus almost free of artefacts.

Compared to insects, not much is known about the spider brain. It is a centralized mass that is situated in the anterior body part of the spider, the prosoma. Within the brain, specific brain centers can be found that process information from different sensory organs. These processing centers are called neuropils and there are 11 bilaterally paired and one unpaired neuropil in the jumping spider brain. Of those neuropils, the unpaired arcuate body and the bilaterally paired mushroom bodies were of particular interest to us, since they are proposed higher-order brain centers, meaning that they integrate information that is received from other brain areas. While both the arcuate body and the mushroom bodies are involved in visual processing in spiders, the arcuate body is assumed to play a role in locomotion control as well.

Figure 3
MicroCT reconstruction of the central nervous system of Marpissa muscosa, including the investigated neuropils (in color); arcuate body (AB, purple), mushroom body pedunculus (MBp, blue), microglomeruli (MG, grey) and the protocerebral neuropil (PN, green).

We found that spiders from the physically enriched treatment had larger absolute brain volumes than spiders from the deprived treatment, while the absolute brain volumes of spiders from the socially enriched treatment lay in between. The relative volume of the mushroom bodies was not significantly different between the treatments, while spiders from a physically enriched environment had enlarged arcuate bodies. Interestingly, an earlier study on the same species showed that spiders from the physically enriched treatment exhibited the strongest exploration tendency. Our finding supports the hypothesis that the arcuate body plays a role in locomotion control in spiders.

All experimental spiders developed larger brains and larger relative arcuate bodies compared to spiders that we caught as adults in the wild. An explanation for this finding might be the regular food supply in the lab compared to the constrained conditions in the wild. Regular food supply may have allowed a higher investment in the development of brain tissue.

Taken together, our study shows that environmental conditions have a strong effect on the development of the spider brain. We demonstrate that neuroplasticity is not limited to vertebrates and insects but is also an integral part of the development of spiders. This plasticity allows them to respond to environmental conditions with adjustments in brain architecture.

Philip O.M. Steinhoff & Gabriele Uhl

 

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