Brain Evolution across the Puerto Rican Anole Radiation

Abstract

Patterns of brain evolution have been widely studied across vertebrates, with the bulk of studies using mammals and/or birds as model systems. Within these groups, species occupying different habitats have been shown to have divergent neuroanatomy, particularly with regard to differences in the relative size of different brain structures, correlated with differences in habitat complexity. We examined the pattern of allometric scaling across the telencephalon, dorsal cortex, dorsomedial cortex, medial cortex, dorsal ventricular ridge, medulla and cerebellum in six species of Puerto Rican Anolis lizards, which are grouped in three distinct ecomorphs (i.e. ecological types) according to interspecific differences in preferred habitat type. The differences in habitat preferences are accompanied by morphological and behavioral adaptations for effective use of each habitat type. Our results challenge this trend and demonstrate a lack of convergence in the relative size of different brain structures between species belonging to the same ecomorph type. Overall brain volume explained between 92.5 and 99.8% of the variance in the volume of each of the brain regions measured and 93.8 and 98.5% of the variance in the volume of each component measured within the telencephalon. This pattern of brain allometry is consistent with concerted brain evolution. However, in the case of the cerebellum, interspecific differences in volume exhibit a trend in accordance with mosaic brain evolution. This suggests that both concerted and mosaic brain evolution have shaped the anole brain, with the former playing a dominant role. Concerted brain evolution is the primary mechanism shaping the brain in mammals and cartilaginous fishes, and its presence in Anolis lizards provides additional evidence supporting the hypothesis that concerted brain evolution might result from a conserved pattern of brain development common to all vertebrates. More generally, our findings highlight the necessity of further studies of brain evolution in reptiles as they can provide valuable insights into the mechanisms underlying vertebrate brain evolution.

Brain Size and Visual Environment Predict Species Differences in Paper Wasp Sensory Processing Brain Regions (Hymenoptera: Vespidae, Polistinae)

“…Optic investment changed more rapidly with brain size than antennal investment in the peripheral sensory neuropils. Although a number of studies have attempted to test between concerted and mosaic brain evolution as alternatives [Barton et al, 1995;Herculano-Houzel, 2011;Powell and Leal, 2012;Gunter and Meyer, 2013;Smaers and Soligo, 2013], our findings suggest that this dichotomy is an oversimplification. Our data suggest that brain size is a key factor to be considered in analysis of brain architecture because brain regions that covary with brain size can do so at different rates [Kaskan et al, 2005].…”

“…Our data did not support the existence of direct trade-offs between sensory modalities. As seen in ants (Formicidae), volumes of optic and antennal regions were positively associated, suggesting concerted brain size effects on evolutionary changes in sensory structure volumes [Gronenberg and Hölldobler, 1999;Powell and Leal, 2012]. Evidence for direct evolutionary trade-offs between brain regions is rarely found [Barton and Harvey, 2000;Gatenby et al, 2011;Warren and Iglesias, 2012].…”

“…First, we tested whether the absolute volumes of the optic and antennal processing regions were negatively correlated. Positive correlations between brain region volumes are expected if evolutionary changes in overall brain size affect all brain regions, and this pattern could mask trade-offs among brain regions [concerted brain evolution: Herculano-Houzel, 2011;Powell and Leal, 2012]. To correct for possible concerted brain size effects, we also tested whether the ratios of volumes of each region to brain remainder were negatively correlated.…”

Evidence for Concerted and Mosaic Brain Evolution in Dragon Lizards

“…Previously, we [Hoops et al, 2016] (and others [Powell and Leal, 2012]) used standard major axis regressions for this type of analysis, but recent evidence suggests that linear models are the preferred statistical method [Kilmer and Rodríguez, 2017;Smith, 2009;Hansen and Bartoszek, 2012]. Again, we centred and standardized the volumetric data for each brain subdivision prior to analysis.…”

“…The classical adaptive radiation studies on ecomorph divergence in Anolis lizards reveal strong, repeated, convergent evolution across island systems [Losos et al, 1998;Langerhans et al, 2006]. Interestingly, while Anolis ecomorphs have evolved many times independently, there is no parallel evolution between ecomorph and brain structure [Powell and Leal, 2012]. In other words, ecomorph does not predict brain structure in Anolis .…”