Early environmental conditions affect the volume of higher-order brain centers in a jumping spider P. O. M. Steinhoff 1 , J. Liedtke 2 , A. Sombke 3 , J. M. Schneider 2 & G. Uhl 1 1 General and Systematic Zoology, Zoological Institute and Museum, University of Greifswald, Greifswald, Germany 2 Biocenter Grindel, Zoological Institute, University of Hamburg, Hamburg, Germany 3 Cytology and Evolutionary Biology, Zoological Institute and Museum, University of Greifswald, Greifswald, Germany Keywords Higher-order brain center; mushroom body; arcuate body; brain volume; neuroplasticity; environmental condition; jumping spiders; Marpissa muscosa. Correspondence Philip O. M. Steinhoff, General and Systematic Zoology, Zoological Institute and Museum, University of Greifswald, Loitzer Strasse 26, 17489 Greifswald, Germany. Tel.: +4915774712207 Email: philipsteinhoff@gmail.com Gabriele Uhl, General and Systematic Zoology, Zoological Institute and Museum, University of Greifswald, Loitzer Strasse 26, 17489 Greifswald, Germany. Tel.: +4938344204242 Email: gabriele.uhl@uni-greifswald.de Editor: Nigel Bennett Received 4 April 2017; revised 30 August 2017; accepted 5 September 2017 doi:10.1111/jzo.12512 Abstract The central nervous system is known to be plastic in volume and structure depending on the stimuli the organism is subjected to. We tested in the jumping spider Marpissa muscosa (Clerck, 1757), whether rearing environments affect the volume of two tar- get higher-order brain centers: the mushroom body (MB) and the arcuate body (AB). We reared female M. muscosa (N = 39) in three environments: solitarily (D: deprived), solitarily but in a physically enriched environment (P: physically enriched) and together with several siblings (G: group). We additionally investigated spiders caught from the field (W: wild). Volumes of MB and AB were compared using microCT analysis. We hypothesized that spiders reared in treatments P and G should have larger MB and AB than the spiders from treatment D, as the enriched environ- ments are presumably cognitively more demanding than the deprived environment. Spiders from treatment P had significantly larger absolute brain volumes than spiders from treatment D, whereas brain volumes of treatment G lay in between. The relative volume of the MB was not significantly different between the treatments, whereas relative AB volumes were significantly larger in treatment P than in D, supporting the hypothesis that the AB is a center of locomotor control. W spiders had smaller absolute brain volumes and relatively smaller AB than spiders from laboratory treat- ments, which suggests developmental constraints under natural, possibly food-limited conditions. Additionally, differences in the relative volume of MB substructures were found. Overall, our study demonstrates that brains of jumping spiders respond plasti- cally to environmental conditions in that absolute brain volume, as well as the rela- tive volume of higher-order brain centers, is affected. Introduction During ontogeny, an organism is exposed to various environ- mental events that may shape its developing nervous system. In fact, neuroplasticity was found to correlate with differences in environmental stimuli and seems to influence behavioral plasticity in many species (Kolb & Whishaw, 1998; Mery & Burns, 2010; Kolb & Gibb, 2014). Most examples of neuro- plasticity come from vertebrate taxa, in which differences in brain volume correlate with rearing environment and learning abilities (Rosenzweig & Bennett, 1996; Moser, 1999; Kih- slinger & Nevitt, 2006; Gogolla, Galimberti & Caroni, 2007; Guay & Iwaniuk, 2008; Burns, Saravanan & Rodd, 2009). Among invertebrates, learning, experience and formation of memory were found to be linked to volume changes of the brain in adult individuals of social hymenoptera (Fahrbach, Strande & Robinson, 1995; Meinertzhagen, 2001; Fahrbach et al., 2003; Giurfa & Sandoz, 2012; Falibene, Roces & R€ ossler, 2015; Yilmaz et al., 2016). A change of volume in brain neuropils responsible for sensory processing, due to a marked change in behavior between juvenile and adult, was also recently found in the spider Deinopis spinosa (Stafstrom, Michalik & Hebets, 2017). Differences in brain size depending on environment and dispersal phase were found in drosophilid flies and locusts (Heisenberg, Heusipp & Wanke, 1995; Ott & Rogers, 2010). Other studies on arthropods investigated devel- opmental plasticity of the brain in response to early environ- mental conditions (Murphey, 1986; Withers, Fahrbach & Robinson, 1993; Heisenberg et al., 1995; Barth et al., 1997; Groh, Tautz & R€ ossler, 2004; Groh, Ahrens & R€ ossler, 2006; Maleszka et al., 2009; Montgomery, Merrill & Ott, 2016). Evi- dence is accumulating that different aspects of the environ- ment, such as its social or physical complexity, may be most relevant for the development and evolution of cognitive abili- ties and the underlying neuronal tissue (e.g. Jolly, 1966; Hum- phrey, 1976; Byrne & Whiten, 1989; Dunbar, 1998; Whiten & van Schaik, 2007; Overington et al., 2009; Farris & Schul- meister, 2011; Heyes, 2012; Farris, 2016; Kamhi et al., 2016). However, it is still strongly debated whether the physical or the social environmental complexity is the main driving force for the evolution of increased cognitive abilities. To address selection on brain development and evolution, either 182 Journal of Zoology 304 (2018) 182–192 ª 2017 The Zoological Society of London Journal of Zoology. Print ISSN 0952-8369