A learning experience elicits sex‐dependent neurogenomic responses in <i>Bicyclus anynana</i> butterflies

Ernst, David A.; Agcaoili, Gabrielle A; Merrill, Abbigail N; Westerman, Erica L.

doi:10.1111/mec.16920

Cited by 3 publications

(5 citation statements)

References 147 publications

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“…Lastly, the MAR-seq analysis of naïve and trained animals points to transcriptomic differences between males and hermaphrodites, particularly within the underlying neuromodulatory network that potentially contributes to the observed behavioral differences. Similar findings have been reported in butterflies, where a genomic analysis revealed a tissue and gene family-specific bias between the sexes that could explain learning dimorphisms 70 . Recent evidence highlights the important role of neuromodulators in recognizing and avoiding PA14 44,48 .…”

Section: Discussionsupporting

confidence: 86%

Modulation by NPYR underlies experience-dependent, sexually dimorphic learning

Peedikayil-Kurien,

Haque,

Gat

et al. 2023

Preprint

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The evolutionary paths taken by each sex within a given species sometimes diverge, resulting in behavioral differences that promote specific fitness outcomes for each sex. Given their distinct needs, the mechanism by which each sex learns from a shared experience is still an open question. We reveal a novel sexual dimorphism in learning: C. elegans males do not learn to avoid the pathogenic bacteria PA14 as efficiently and rapidly as hermaphrodites, even though their innate immunity recognizes the pathogen in a similar manner. Notably, we observe sexually dimorphic neuronal activity following pathogen exposure: hermaphrodites generate robust representations while males, in line with their behavior, exhibit contrasting representations, suggesting that a mechanism that modulates incoming sensory cues is at play. Transcriptomic and behavioral analysis revealed that the neuropeptide receptor npr-5, an ortholog of the mammalian NPY receptor, regulates male learning by modulating neuronal activity. Furthermore, we show the dependency of the males decision-making phenotype on their sexual status and demonstrate the pivotal role of npr-5 in this regulation as a sensory gatekeeper. Thus, collectively, we portray sex-specific plasticity in behavior toward a shared experience by modulating learning to fulfill the evolutionary needs.

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Section: Discussionsupporting

confidence: 86%

Modulation by NPYR underlies experience-dependent, sexually dimorphic learning

Peedikayil-Kurien,

Haque,

Gat

et al. 2023

Preprint

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“…Additionally, compared to a previous B. anynana study that investigated the gene expression networks behind sexually dimorphic imprinting-like learning [34], we found nine shared DEGs, including the rotatin-like protein ( RTTN/Ana3 ), which is needed for the maintenance of sensory neurons [96,97]. RTTN/Ana3 is also linked to human neurodegenerative diseases such as polymicrogyria and microcephaly, which can lead to learning disabilities in humans and mice [98–105] (Fig 4).…”

Section: Discussionmentioning

confidence: 99%

“…Female and male B. anynana butterflies learn mate preferences for visual signals if they are exposed to sexually mature individuals of the opposite sex shortly after emergence from chrysalis, a time when neither males nor females are ready to mate in this species [31]. Specific to females, naïve females prefer males with two dorsal forewing eyespots, however females exposed to males with four dorsal forewing eyespots immediately following emergence prefer four spot males over two spot males in later mating trials [16,[32][33][34]. Past studies using B. anynana to investigate visual imprinting-like learning, as well as the associated brain gene expression, have typically used three hours as the exposure period.…”

Section: Introductionmentioning

confidence: 99%

“…To address these gaps in literature, we used the butterfly Bicyclus anynana to examine the temporal dynamics behind imprinting-like learning and its associated gene expression [31]. Specific to females, naïve females prefer males with two dorsal forewing eyespots, however females exposed to males with four dorsal forewing eyespots immediately following emergence prefer four spot males over two spot males in later mating trials [16,[32][33][34]. Past studies using B. anynana to investigate visual imprinting-like learning, as well as the associated brain gene expression, have typically used three hours as the exposure period.…”

Section: Introductionmentioning

confidence: 99%

“…Neurogenomically, transcriptional changes responsible for long-term memory formation are initiated shortly after exposure in all animal systems studied to date [22,26,27]. Therefore, by only assessing transcriptional change at the end of a three-hour (or any lengthy exposure) period [34], we are likely missing genes critically important to mate preference learning and memory, which would better help us understand the mechanistic similarities between imprinting-like learning and associative learning in general. Therefore, in this study we examined the effect of increasing exposure time on learning ability by exposing naïve females to 4-spotted males for five different time periods (i.e.…”

Section: Introductionmentioning

confidence: 99%

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Asynchronous temporal variance in learning behaviour and neural gene expression in a butterfly

Ter,

Westerman

2024

Preprint

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Mate preference learning, including imprinting-like learning, is pervasive across animal taxa, and can affect the selection and maintenance of certain phenotypes. However, not much is known about the temporal dynamics behind imprinting-like learning, or the genetic underpinnings underlying it. To uncover the temporal dynamics of imprinting-like learning, from both a behavioural and transcriptional perspective, we conducted learning and RNA-Seq time series using the butterfly Bicyclus anynana, a species where both sexes learn mate preferences. We exposed females to an unfamiliar, unpreferred male phenotype (4-spotted male) for five different exposure (training) periods, ranging from 30 minutes to three hours, and recorded their choice between the preferred, familiar male phenotype (2-spotted) and 4-spotted males in mate choice trials conducted two days after training. We also assessed differential gene expression of naive females and females exposed to trainer males for these same five exposure periods, to identify temporal patterns in gene expression associated with learning. While we found that the longest exposure had the strongest effect on preference learning, we did not observe a linear effect of exposure time on learning. We also show that the highest peak of differentially expressed genes (DEGs) was after one hour of exposure. While a number of genes were uniquely DE at each time point, one gene, associated with transcription initiation, was differentially expressed during learning across all five time points. We observed a similar decreasing trend in both gene expression and learned response after 1.5 hours of exposure, offering new insights to possible attention and forgetting mechanisms. Therefore, our results indicate that both gene expression and learning are temporally dynamic, and not linear through time. They also highlight the role of transcription in mate preference learning and memory formation in Lepidoptera, and illustrate that imprinting-like learning may exhibit similar molecular temporal dynamics as associative learning.

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