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Neural divergence and hybrid disruption between ecologically isolated
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Heliconius butterflies
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Stephen H. Montgomery1,2, Matteo Rossi2,3, W. Owen McMillan2, Richard M. Merrill2,3
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School of Biological Science, University of Bristol, 24 Tyndall Avenue, Bristol, UK, BS8 1TQ
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Smithsonian Tropical Research Institute, Gamboa, Panama
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Division of Evolutionary Biology, Ludwig-Maximilians-Universität, München, Germany
Affiliations
Correspondence:
[email protected]
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Summary
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The importance of behavioural evolution during speciation is well established, but we know little
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about how this is manifest in sensory and neural systems. Although a handful of studies have
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linked specific neural changes to divergence in host or mate preferences associated with
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speciation, how brains respond to broad environmental transitions, and whether this contributes
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to reproductive isolation, remains unknown. Here, we examine divergence in brain morphology
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and neural gene expression between closely related, but ecologically distinct, Heliconius
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butterflies. Despite on-going gene flow, sympatric species pairs within the melpomene-cydno
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complex are consistently separated across a gradient of open to closed forest and decreasing
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light intensity. By generating quantitative neuroanatomical data for 107 butterflies, we show that
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H. melpomene and H. cydno have substantial shifts in brain morphology across their geographic
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range, with divergent structures clustered in the visual system. These neuroanatomical
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differences are mirrored by extensive divergence in neural gene expression. Differences in both
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morphology and gene expression are heritable, exceed expected rates of neutral divergence, and
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result in intermediate traits in first generation hybrid offspring. This likely disrupts neural system
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function, leading to a mismatch between the environment and the behavioral response of hybrids.
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Our results suggest that disruptive selection on both neural function and external morphology
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result in coincident barriers to gene flow, thereby facilitating speciation.
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Keywords:
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Brain evolution, ecological speciation, neuroecology, niche partitioning, reproductive isolation
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bioRxiv preprint doi: https://doi.org/10.1101/2020.07.01.182337. this version posted July 2, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. It is made available under a CC-BY-NC-ND 4.0 International license.
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Introduction
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Ecological adaptation is a major force driving the evolution of new species [1,2]. Although it is
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well established that divergent selection can influence behavioural traits and promote speciation
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[3], there are few empirical examples of how divergent selection acts on the underlying sensory
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and neural systems. For example, existing studies on adaptation across divergent light regimes
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have largely focused on the peripheral sensory systems, often in the context of divergent mate
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preference [4,5]. However, sensory perception is only the first of many mechanisms within the
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nervous systems that may experience divergent selection, and mating preferences are only one
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of many behaviours that may that can be affected by the environment, and consequently
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contribute to reproductive isolation. Behavioural challenges imposed by novel environments can
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instead be met by changes in how sensory information is processed, often reflected in differential
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investment in brain components that refines the sensitivity, acuity to, or integration of, different
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stimuli.
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The intimate relationship between brain structure and ecology is apparent in many
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comparative studies of neuroanatomy. For example, the expansion of visual pathways in primates
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[6], cerebellar expansion and refinement of the exterolateral nucleus in electric fish [7–9], the
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contrasting adaptations of diurnal and nocturnal lifestyles in hawk moths [10], and the
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independent colonization of cave systems that underlie the radiation in Mexican cavefish [11], all
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indicate the importance of neuroanatomical adaptations to contrasting ecological needs.
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However, these comparative studies generally focus on phylogenetically distinct comparisons
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across relatively distantly related species. At the other extreme, several studies considering inter-
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specific variation across populations, or between eco-morphs, instead highlight the potential for
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plasticity in brain development to optimize brain structure and function to local conditions [12–14].
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Between these population and phylogenetic levels there is a scarcity of information about
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the role brains play in facilitating speciation across environmental gradients, either through
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developmental plasticity or the accumulation of heritable changes during ecological divergence.
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Hence, whether evolutionary changes in neural systems play a causative role in ecological
