Plasticity and genetic effects contribute to different axes of neural divergence in a community of mimetic Heliconius butterflies

Abstract

Changes in ecological preference, often driven by spatial and temporal variation in resource distribution, can expose populations to environments with divergent information content. This can lead to adaptive changes in the degree to which individuals invest in sensory systems and downstream processes, to optimize behavioural performance in different contexts. At the same time, environmental conditions can produce plastic responses in nervous system development and maturation, providing an alternative route to integrating neural and ecological variation. Here, we explore how these two processes play out across a community of Heliconius butterflies. Heliconius communities exhibit multiple Mullerian mimicry rings, associated with habitat partitioning across environmental gradients. These environmental differences have previously been linked to heritable divergence in brain morphology in parapatric species pairs. They also exhibit a unique dietary adaptation, known as pollen feeding, that relies heavily on learning foraging routes, or trap‐lines, between resources, which implies an important environmental influence on behavioural development. By comparing brain morphology across 133 wild‐caught and insectary‐reared individuals from seven Heliconius species, we find strong evidence for interspecific variation in patterns of neural investment. These largely fall into two distinct patterns of variation; first, we find consistent patterns of divergence in the size of visual brain components across both wild and insectary‐reared individuals, suggesting genetically encoded divergence in the visual pathway. Second, we find interspecific differences in mushroom body size, a central component of learning and memory systems, but only among wild caught individuals. The lack of this effect in common‐garden individuals suggests an extensive role for developmental plasticity in interspecific variation in the wild. Finally, we illustrate the impact of relatively small‐scale spatial effects on mushroom body plasticity by performing experiments altering the cage size and structure experienced by individual H. hecale. Our data provide a comprehensive survey of community level variation in brain structure, and demonstrate that genetic effects and developmental plasticity contribute to different axes of interspecific neural variation.

Multiple axes of visual system diversity in Ithomiini, an ecologically diverse tribe of mimetic butterflies

“…For example, a comparison of two Boloria butterfly species identified larger eyes and facets in the frontal eye region in B. aquilonaris , whose habitat is naturally fragmented relative to B. eunomia , suggesting that differences in eye morphology can evolve remarkably rapidly in response to ecological challenges ( Turlure et al, 2016 ). Consistent patterns of neural divergence in response to ecological preference shifts have also been observed between parapatric Heliconius butterfly species, which also display eye structural variation, separated across continuous environmental gradients within tropical forests ( Hebberecht et al, 2023 ; Montgomery and Merrill, 2017 ; Montgomery et al, 2021 ; Seymoure et al, 2015 ).…”

Adult neurogenesis does not explain the extensive post-eclosion growth ofHeliconiusmushroom bodies

“…Associated with this behaviour, they also have the largest mushroom bodies of any Lepidoptera described to date [ 34 , 35 ]. Previous analyses have established a significant influence of age and environmental effects on mushroom body size in Heliconius [ 33 , 36 ]. Here, we contribute two advances to our understanding of this system.…”

“…Within this Neotropical tribe, Heliconius have mushroom bodies that are up to four times larger than other Heliconiini genera, relative to overall brain size [ 32 – 34 ], and the largest described in any lepidoptera [ 34 , 35 ]. In addition, both age- and environment-dependent plasticity are linked to volumetric increases in the mushroom bodies [ 33 ], which show a consistently high degree of plasticity across Heliconius compared to other brain regions [ 36 ]. The likely behavioural relevance of this mushroom body expansion is a unique dietary innovation, whereby adult Heliconius collect and digest pollen from a restricted range of floral plants [ 37 , 38 ].…”

Monarch butterflies memorize the spatial location of a food source

“…This means that not only Heliconius but also migratory monarch butterflies overwintering in Mexico take off for their foraging bouts from the same location daily. The brains of monarch butterflies [74] and Heliconius [75,76] have prominent mushroom bodies, and more recent phylogenetic analysis in Heliconius revealed a correlation between mushroom body size and the evolution of pollen feeding, a dietary innovation accompanied with an extensive spatial memory [37]. As brain regions involved in associative learning, neurons of the mushroom bodies likely encode visual memories and associate a valence signal, i.e.…”