Patterns of visual adaptation in tropical mimetic butterflies

Species diversity within an ecosystem can be supported by favouring microhabitat specialisation. In complex habitats, like tropical rainforests, spatial and temporal segregation across microhabitats can expose species to distinct sensory realms. For many animals, visual systems serve as the primary conduit for perceiving biologically relevant sensory information, and the structural and functional variety of eyes and sensory brain regions reflects their critical role in diverse animal behaviours. However, little is known of their role in mediating niche segregation across subtle ecological scales, particularly in terrestrial environments. I explore the role of microhabitat partitioning in driving predictable patterns of adaptive visual system evolution within two diverse radiations of mimetic Neotropical butterfly, the Heliconius and Ithomiini. By taking a comparative approach, I investigate whether dual patterns of habitat divergence and convergence is manifested in the visual system at the perceptual, processing, and molecular level. I find extensive evidence of heritable, habitat-associated visual system variation, particularly for neural processing structures, hinting at the evolutionary lability of these systems to rapidly accommodate local adaptations to visual ecologies. My research also empirically demonstrates, for the first time, how variation in forest structure can give rise to distinct photic environments, highlighting the role of spectral variation as a major driver of adaptive community assemblage within a terrestrial forest radiation. In addition, evidence of visual morphological convergence offers a mechanistic insight into the evolvability of visual adaptations when confronted with similar ecological challenges, shedding light on their significance in promoting ecological diversification and speciation

Neuroanatomical shifts mirror patterns of ecological divergence in three diverse clades of mimetic butterflies

Microhabitat partitioning in heterogenous environments can support more diverse communities but may expose partitioned species to distinct perceptual challenges. Divergence across microhabitats could therefore lead to local adaptation to contrasting sensory conditions across small spatial scales, but this aspect of community structuring is rarely explored. Diverse communities of ithomiine butterflies provide an example where closely related species partition tropical forests, where shifts in mimetic coloration are tightly associated with shifts in habitat preference. We test the hypothesis that these mimetic and ecological shifts are associated with distinct patterns of sensory neural investment by comparing brain structure across 164 individuals of 16 species from three ithomiine clades. We find distinct brain morphologies between Oleriina and Hypothyris, which are mimetically homogenous and occupy a single microhabitat. Oleriina, which occurs in low‐light microhabitats, invests less in visual brain regions than Hypothyris, with one notable exception, Hyposcada anchiala, the only Oleriina sampled to have converged on mimicry rings found in Hypothyris. We also find that Napeogenes, which has diversified into a range of mimicry rings, shows intermediate patterns of sensory investment. We identify flight height as a critical factor shaping neuroanatomical diversity, with species that fly higher in the canopy investing more in visual structures. Our work suggests that the sensory ecology of species may be impacted by, and interact with, the ways in which communities of closely related organisms are adaptively assembled

A 13-year record of erosion on badland sites in the Karoo, South Africa

Land degradation in South Africa has been of concern for more than 100 years with both climate change and inappropriate land management (overgrazing) being proposed as primary drivers. However, there are few quantitative studies of degradation and, in particular, few of erosion by water. Badlands, taken here to be the landform which results from extreme erosion, have been notably neglected. We report on 13 consecutive years of erosion pin measurements of badland erosion on 10 study sites in the Sneeuberg uplands of the eastern Karoo in South Africa. The study sites are on Holocene colluvium which mantles footslopes. They have been subject to overgrazing for at least 100 years, c. 1850–1950. Currently they are lightly grazed by sheep. The area receives about 500 mm rainfall per year. The sites are remote, with only informal, farmer-operated, daily raingauges nearby. The nearest subdaily raingauge is c. 55 km distant. Also we report on an analysis of the erosion pin data which focuses on establishing the origins and context of the badlands, including the relationship between study sites and adjacent valley-bottom gully systems; compare erosion rates on our study sites with rates determined by erosion pins on other badland sites; and discuss the implications of these erosion rates for landscape development and off-site impacts. Net erosion rates on the study sites are relatively high compared with global badland rates and range from 3.1 to 8.5 mm yr-1 which may be extrapolated to 53 to 145 t ha yr-1 (using a measured bulk density of 1.7 g cm-3). However, comparisons with badland sites elsewhere are difficult because of different measuring methodologies, lithologies, climate and dominant processes. Erosion rates on the study sites are strongly influenced by rainfall amounts and, in particular, by daily rainfall events which exceed ~10 mm: this is the threshold intensity at which runoff has been observed to commence on badlands. Of significance, but of lesser influence, is weathering, mainly by wetting and drying: this prepares bare surfaces for erosion. However, questions remain regarding the role of site characteristics, and of processes at each site, in determining between-site differences in erosion rate. Crude extrapolation of current rates of erosion, in conjunction with depths of incision into the badlands, suggests that badland development started around 200 years ago, probably as a response to the introduction of European-style stock farming which resulted in overgrazing. We assume, but cannot quantify, the additional influence of periods of drought and burning in the erosional history of the area. Intermittent connection of these badlands to valley-bottom gullies and therefore to small farm dams and ultimately to large water storage reservoirs increases their impact on local water resources

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

Funder: Smithsonian Tropical Research Institute; doi: http://dx.doi.org/10.13039/100009201Changes 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