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Novel brain gene-expression patterns are associated with a novel predaceous behaviour in tadpoles

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Cris C. Ledón-Rettig
Cris C. Ledón-Rettig
Cris C. Ledón-Rettig
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Abstract

Novel behaviours can spur evolutionary change and sometimes even precede morphological innovation, but the evolutionary and developmental contexts for their origins can be elusive. One proposed mechanism to generate behavioural innovation is a shift in the developmental timing of gene-expression patterns underlying an ancestral behaviour, or molecular heterochrony. Alternatively, novel suites of gene expression, which could provide new contexts for signalling pathways with conserved behavioural functions, could promote novel behavioural variation. To determine the relative contributions of these alternatives to behavioural innovation, I used a species of spadefoot toad, Spea bombifrons . Based on environmental cues, Spea larvae develop as either of two morphs: ‘omnivores' that, like their ancestors, feed on detritus, or ‘carnivores' that are predaceous and cannibalistic. Because all anuran larvae undergo a natural transition to obligate carnivory during metamorphosis, it has been proposed that the novel, predaceous behaviour in Spea larvae represents the accelerated activation of gene networks influencing post-metamorphic behaviours. Based on comparisons of brain transcriptional profiles, my results reject widespread heterochrony as a mechanism promoting the expression of predaceous larval behaviour. They instead suggest that the evolution of this trait relied on novel patterns of gene expression that include components of pathways with conserved behavioural functions.
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Cite this article: Ledón-Rettig CC. 2021 Novel
brain gene-expression patterns are associated
with a novel predaceous behaviour in tadpoles.
Proc. R. Soc. B 288: 20210079.
https://doi.org/10.1098/rspb.2021.0079
Received: 12 January 2021
Accepted: 2 March 2021
Subject Category:
Evolution
Subject Areas:
behaviour, developmental biology, evolution
Keywords:
carnivory, transcriptomics, plasticity,
polyphenism, cannibalism
Author for correspondence:
Cris C. Ledón-Rettig
e-mail: crisledo@indiana.edu
Electronic supplementary material is available
online at https://doi.org/10.6084/m9.figshare.
c.5347579.
Novel brain gene-expression patterns are
associated with a novel predaceous
behaviour in tadpoles
Cris C. Ledón-Rettig
Department of Biology, Indiana University, 915 E. Third Street, Myers Hall 100, Bloomington, IN 47405-7107,
USA
CCL-R, 0000-0002-1417-7486
Novel behaviours can spur evolutionary change and sometimes even
precede morphological innovation, but the evolutionary and developmental
contexts for their origins can be elusive. One proposed mechanism to gener-
ate behavioural innovation is a shift in the developmental timing of
gene-expression patterns underlying an ancestral behaviour, or molecular
heterochrony. Alternatively, novel suites of gene expression, which could
provide new contexts for signalling pathways with conserved behavioural
functions, could promote novel behavioural variation. To determine the rela-
tive contributions of these alternatives to behavioural innovation, I used a
species of spadefoot toad, Spea bombifrons. Based on environmental cues,
Spea larvae develop as either of two morphs: ‘omnivores’that, like their
ancestors, feed on detritus, or ‘carnivores’that are predaceous and canniba-
listic. Because all anuran larvae undergo a natural transition to obligate
carnivory during metamorphosis, it has been proposed that the novel,
predaceous behaviour in Spea larvae represents the accelerated activation
of gene networks influencing post-metamorphic behaviours. Based on com-
parisons of brain transcriptional profiles, my results reject widespread
heterochrony as a mechanism promoting the expression of predaceous
larval behaviour. They instead suggest that the evolution of this trait
relied on novel patterns of gene expression that include components of
pathways with conserved behavioural functions.
1. Introduction
Novel behaviours can precede and even shape morphological evolution [1,2].
Although several theoretical frameworks have been proposed to explain the
evolution of novel traits [3–6], relatively few empirical studies attempt to use
such frameworks to explain the evolution of novel behaviours [7–9]. Therefore,
an outstanding question is where the raw material for evolutionarily novel
behaviours comes from.
A major mechanism proposed as a catalyst for behavioural innovation is
heterochrony, whereby novel traits arise from shifts in the ontogenetic
(i.e. developmental) timing of the expression of ancestral traits [4,10]. The ‘mol-
ecular heterochrony hypothesis’specifically predicts that gene expression
associated with an ancestral behaviour will also be associated with a derived
behaviour, albeit during a different stage of development [11]. For example,
sibling care, a behavioural innovation and hallmark trait of eusocial systems,
may have evolved from the precocious display of maternal care in worker
females towards siblings instead of their own offspring [12]. Indeed, a suite of
common genes have been implicated in both sibling and maternal care behaviour
in Polistes wasps [13].
However, other studies have suggested the importance of a genetic ‘toolkit’
in the evolution of sibling care [14]. This alternative hypothesis posits that cer-
tain genes and pathways have highly conserved roles in behaviour across
diverse taxa, and that novel, complex behaviours can be assembled anew
from simpler, pre-existing behavioural modules [8]. Supporting this scenario,
© 2021 The Author(s) Published by the Royal Society. All rights reserved.
... Indeed, we found that the set of genes showing plasticity in S. multiplicata, but not showing it in P. cultripes, is enriched for major organismal, head, and brain development terms. These data are therefore consistent with previous studies, which have shown that carnivores differ from omnivores behaviorally (Pfennig, 1999;Pfennig et al., 1993;Pomeroy, 1981), morphologically (Levis et al., 2018;Martin & Pfennig, 2009;Pfennig, 1992b;Pfennig & Murphy, 2000, and physiologically (Ledón-Rettig, 2021;Ledón-Rettig et al., 2008. Thus, it makes sense that extensive lineage-specific gene expression plasticity has evolved in Spea's polyphenism when compared to the relatively simple plasticity of developmental acceleration in Pelobates. ...
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... Generally, changes in the brain are associated with a dynamic (enriched) environment and can be important for learning, memory and behaviour [56][57][58]. Thus, a shift to the dynamic cue environment may have caused changes in the brain to cope with social interactions in that environment [59]. These changes were then further enhanced in those individuals who were best suited for that dynamic social environmentcarnivores (electronic supplementary material, figure S1). ...
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... Such changes in brain gene expression are common in organisms encountering a dynamic or enriched environment (Abbey- Lee et al., 2018;Chesler & Williams 2004;Rampon et al., 2000) and are generally consistent with previous work on brain gene expression between spadefoot morphs (Ledón-Rettig, 2021). Our results suggest that the individuals that have more to gain from effectively navigating such a dynamic environment-carnivores-may do so by expanding their nervous system (presumably the brain) and increasing their activity to facilitate changes in behavior accompanying a predatory lifestyle (Ledón-Rettig, 2021;Pfennig, 1999;Pfennig & Murphy, 2000). The prevalence of neurological disease terms in omnivore-biased genes further supports differences between morphs in cognitive function and capacity to navigate a complex environment with diverse resources and socially antagonistic interactions. ...
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