Modality-specific long-term memory enhancement in Heliconius butterflies
How animals perceive, process and respond to environmental cues is tightly tuned to species-specific ecological demands and reflected by the structure of neural systems. In the Neotropical butterflies, , the mushroom bodies, insect learning and memory centres are significantly expanded compared with...
Saved in:
| Published in: | Philosophical transactions of the Royal Society of London. Series B. Biological sciences Vol. 380; no. 1929; p. 20240119 |
|---|---|
| Main Authors: | , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
England
26.06.2025
|
| Subjects: | |
| ISSN: | 1471-2970, 1471-2970 |
| Online Access: | Get more information |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| Abstract | How animals perceive, process and respond to environmental cues is tightly tuned to species-specific ecological demands and reflected by the structure of neural systems. In the Neotropical butterflies,
, the mushroom bodies, insect learning and memory centres are significantly expanded compared with their closest relatives. This expansion coincided with the evolution of a novel diet of pollen and the ability to learn spatial foraging routes. Previous research has shown that
have more accurate long-term visual memory than other Heliconiini. Here, we test whether this enhanced memory stability is specific to visual contexts by conducting a long-term olfactory memory assay in two
species and two outgroup species. We found no difference in long-term olfactory memory between
and outgroup Heliconiini, and combining data from olfactory and visual memory trials confirmed a modality-specific improvement in memory recall in
. Tests of how Heliconiini species prioritize olfactory and visual cues when presented in conflict show no consistent pattern, suggesting that variation in memory stability is not explained by inter-specific differences in attentiveness to sensory cues. Our data provide a rare case where memory performance has been compared across species and sensory modalities to identify evidence of a modality-specific shift.This article is part of the Theo Murphy meeting issue 'Selection shapes diverse animal minds'. |
|---|---|
| AbstractList | How animals perceive, process and respond to environmental cues is tightly tuned to species-specific ecological demands and reflected by the structure of neural systems. In the Neotropical butterflies, Heliconius, the mushroom bodies, insect learning and memory centres are significantly expanded compared with their closest relatives. This expansion coincided with the evolution of a novel diet of pollen and the ability to learn spatial foraging routes. Previous research has shown that Heliconius have more accurate long-term visual memory than other Heliconiini. Here, we test whether this enhanced memory stability is specific to visual contexts by conducting a long-term olfactory memory assay in two Heliconius species and two outgroup species. We found no difference in long-term olfactory memory between Heliconius and outgroup Heliconiini, and combining data from olfactory and visual memory trials confirmed a modality-specific improvement in memory recall in Heliconius. Tests of how Heliconiini species prioritize olfactory and visual cues when presented in conflict show no consistent pattern, suggesting that variation in memory stability is not explained by inter-specific differences in attentiveness to sensory cues. Our data provide a rare case where memory performance has been compared across species and sensory modalities to identify evidence of a modality-specific shift.This article is part of the Theo Murphy meeting issue 'Selection shapes diverse animal minds'.How animals perceive, process and respond to environmental cues is tightly tuned to species-specific ecological demands and reflected by the structure of neural systems. In the Neotropical butterflies, Heliconius, the mushroom bodies, insect learning and memory centres are significantly expanded compared with their closest relatives. This expansion coincided with the evolution of a novel diet of pollen and the ability to learn spatial foraging routes. Previous research has shown that Heliconius have more accurate long-term visual memory than other Heliconiini. Here, we test whether this enhanced memory stability is specific to visual contexts by conducting a long-term olfactory memory assay in two Heliconius species and two outgroup species. We found no difference in long-term olfactory memory between Heliconius and outgroup Heliconiini, and combining data from olfactory and visual memory trials confirmed a modality-specific improvement in memory recall in Heliconius. Tests of how Heliconiini species prioritize olfactory and visual cues when presented in conflict show no consistent pattern, suggesting that variation in memory stability is not explained by inter-specific differences in attentiveness to sensory cues. Our data provide a rare case where memory performance has been compared across species and sensory modalities to identify evidence of a modality-specific shift.This article is part of the Theo Murphy meeting issue 'Selection shapes diverse animal minds'. How animals perceive, process and respond to environmental cues is tightly tuned to species-specific ecological demands and reflected by the structure of neural systems. In the Neotropical butterflies, , the mushroom bodies, insect learning and memory centres are significantly expanded compared with their closest relatives. This expansion coincided with the evolution of a novel diet of pollen and the ability to learn spatial foraging routes. Previous research has shown that have more accurate long-term visual memory than other Heliconiini. Here, we test whether this enhanced memory stability is specific to visual contexts by conducting a long-term olfactory memory assay in two species and two outgroup species. We found no difference in long-term olfactory memory between and outgroup Heliconiini, and combining data from olfactory and visual memory trials confirmed a modality-specific improvement in memory recall in . Tests of how Heliconiini species prioritize olfactory and visual cues when presented in conflict show no consistent pattern, suggesting that variation in memory stability is not explained by inter-specific differences in attentiveness to sensory cues. Our data provide a rare case where memory performance has been compared across species and sensory modalities to identify evidence of a modality-specific shift.This article is part of the Theo Murphy meeting issue 'Selection shapes diverse animal minds'. |
| Author | Farnworth, Max S McMillan, W Owen Alcalde Anton, Amaia Margereth Aguilar, Jane Dalbosco Dell'Aglio, Denise Hernández, Greta Hodge, Elizabeth A Bestea, Louise Montgomery, Stephen H |
| Author_xml | – sequence: 1 givenname: Elizabeth A orcidid: 0009-0001-1837-4719 surname: Hodge fullname: Hodge, Elizabeth A organization: Smithsonian Tropical Research Institute, Panama City 0843-03092, Panama – sequence: 2 givenname: Amaia orcidid: 0000-0002-2091-258X surname: Alcalde Anton fullname: Alcalde Anton, Amaia organization: Smithsonian Tropical Research Institute, Panama City 0843-03092, Panama – sequence: 3 givenname: Louise orcidid: 0000-0002-0440-1122 surname: Bestea fullname: Bestea, Louise organization: Smithsonian Tropical Research Institute, Panama City 0843-03092, Panama – sequence: 4 givenname: Greta orcidid: 0000-0002-7560-5114 surname: Hernández fullname: Hernández, Greta organization: Smithsonian Tropical Research Institute, Panama City 0843-03092, Panama – sequence: 5 givenname: Jane surname: Margereth Aguilar fullname: Margereth Aguilar, Jane organization: Smithsonian Tropical Research Institute, Panama City 0843-03092, Panama – sequence: 6 givenname: Max S orcidid: 0000-0003-2418-3203 surname: Farnworth fullname: Farnworth, Max S organization: School of Biological Sciences, University of Bristol, Bristol BS8 1TQ, UK – sequence: 7 givenname: Denise orcidid: 0000-0002-2854-7054 surname: Dalbosco Dell'Aglio fullname: Dalbosco Dell'Aglio, Denise organization: Smithsonian Tropical Research Institute, Panama City 0843-03092, Panama – sequence: 8 givenname: W Owen orcidid: 0000-0003-2805-2745 surname: McMillan fullname: McMillan, W Owen organization: Smithsonian Tropical Research Institute, Panama City 0843-03092, Panama – sequence: 9 givenname: Stephen H orcidid: 0000-0002-5474-5695 surname: Montgomery fullname: Montgomery, Stephen H organization: Smithsonian Tropical Research Institute, Panama City 0843-03092, Panama |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/40566908$$D View this record in MEDLINE/PubMed |
| BookMark | eNpNjztPwzAYRS1URB-wMqKMLCm248TxiCqgSEUsMEd-fAYjP0rsDP33VKJIDFfnDkdXuks0iykCQtcErwkW_d2Yi1pTTNkaEyLO0IIwTmoqOJ7963O0zPkLYyxazi7QnOG26wTuF2j7koz0rhzqvAftrNOVT_GjLjCGKkBI46GC-CmjhgCxVC5WW_BOp-imXKmpHEXrHeRLdG6lz3B14gq9Pz68bbb17vXpeXO_qzVreKmFpFpZsFh1xAhQYLUynBnobMd7zNuGAZZKS6IZ8P4Y03caMypV18re0BW6_d3dj-l7glyG4LIG72WENOWhoZTRVrCGHNWbkzqpAGbYjy7I8TD8vac_jPpgDQ |
| CitedBy_id | crossref_primary_10_1098_rstb_2024_0110 crossref_primary_10_1098_rstb_2024_0255 crossref_primary_10_1098_rstb_2024_0108 |
| ContentType | Journal Article |
| DBID | CGR CUY CVF ECM EIF NPM 7X8 |
| DOI | 10.1098/rstb.2024.0119 |
| DatabaseName | Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed MEDLINE - Academic |
| DatabaseTitle | MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) MEDLINE - Academic |
| DatabaseTitleList | MEDLINE - Academic MEDLINE |
| Database_xml | – sequence: 1 dbid: NPM name: PubMed url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 2 dbid: 7X8 name: MEDLINE - Academic url: https://search.proquest.com/medline sourceTypes: Aggregation Database |
| DeliveryMethod | no_fulltext_linktorsrc |
| Discipline | Medicine Sciences (General) Biology |
| EISSN | 1471-2970 |
| ExternalDocumentID | 40566908 |
| Genre | Journal Article |
| GrantInformation_xml | – fundername: European Research Council – fundername: Smithsonian Tropical Research Institute – fundername: Natural Environment Research Council |
| GroupedDBID | --- -~X 0R~ 2WC 4.4 53G AACGO AANCE ABPLY ABTLG ACPRK ADBBV AFRAH ALMA_UNASSIGNED_HOLDINGS AOIJS BAWUL BTFSW CGR CUY CVF E3Z EBS ECM EIF F5P GX1 H13 HZ~ JSG JST KQ8 MRS MV1 NPM NSAHA O9- OK1 RPM RRY TN5 V1E YNT ~02 7X8 |
| ID | FETCH-LOGICAL-c437t-9a2cbfef0b61d9ebefcbd74de6f67807534e0abca1c4e784e7d86c042ab65a8d2 |
| IEDL.DBID | 7X8 |
| ISICitedReferencesCount | 3 |
| ISICitedReferencesURI | http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=001517012300013&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D |
| ISSN | 1471-2970 |
| IngestDate | Thu Jun 26 17:31:22 EDT 2025 Fri Jul 04 01:55:47 EDT 2025 |
| IsDoiOpenAccess | false |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 1929 |
| Keywords | vision olfaction learning Heliconiini associative memory mushroom body |
| Language | English |
| LinkModel | DirectLink |
| MergedId | FETCHMERGED-LOGICAL-c437t-9a2cbfef0b61d9ebefcbd74de6f67807534e0abca1c4e784e7d86c042ab65a8d2 |
| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
| ORCID | 0000-0003-2418-3203 0000-0002-7560-5114 0000-0003-2805-2745 0000-0002-5474-5695 0000-0002-2091-258X 0000-0002-0440-1122 0000-0002-2854-7054 0009-0001-1837-4719 |
| OpenAccessLink | https://pubmed.ncbi.nlm.nih.gov/PMC12198899 |
| PMID | 40566908 |
| PQID | 3224259431 |
| PQPubID | 23479 |
| ParticipantIDs | proquest_miscellaneous_3224259431 pubmed_primary_40566908 |
| PublicationCentury | 2000 |
| PublicationDate | 2025-Jun-26 20250626 |
| PublicationDateYYYYMMDD | 2025-06-26 |
| PublicationDate_xml | – month: 06 year: 2025 text: 2025-Jun-26 day: 26 |
| PublicationDecade | 2020 |
| PublicationPlace | England |
| PublicationPlace_xml | – name: England |
| PublicationTitle | Philosophical transactions of the Royal Society of London. Series B. Biological sciences |
| PublicationTitleAlternate | Philos Trans R Soc Lond B Biol Sci |
| PublicationYear | 2025 |
| SSID | ssj0009574 |
| Score | 2.501924 |
| Snippet | How animals perceive, process and respond to environmental cues is tightly tuned to species-specific ecological demands and reflected by the structure of... |
| SourceID | proquest pubmed |
| SourceType | Aggregation Database Index Database |
| StartPage | 20240119 |
| SubjectTerms | Animals Butterflies - physiology Cues Memory, Long-Term Olfactory Perception Smell Species Specificity Visual Perception |
| Title | Modality-specific long-term memory enhancement in Heliconius butterflies |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/40566908 https://www.proquest.com/docview/3224259431 |
| Volume | 380 |
| WOSCitedRecordID | wos001517012300013&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D |
| hasFullText | |
| inHoldings | 1 |
| isFullTextHit | |
| isPrint | |
| link | http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV07T8MwED7xFgvQ8n7JSAwwmKaxazsTQoiqA606AOoW2Y4DlSAppCDx7zkn4bEgITEkW6TI993d5zv7O4Bj5phvtikqjVOUMy6pFs5QzSVjXHR0Ut7wvruWg4EajaJhXXAr6mOVnzGxDNRJbn2NvIXAQ3hFmO_OJ8_UT43y3dV6hMYszDOkMh7VcqR-iO6WKsxtDMA0jGTwJdqoWkitDO4OQ37mRc9-p5dlmumu_vcH12ClJpjkokJEA2Zc1oTFauTkexOW-nUzvQmN2q8LclKLT5-uQ6-fJyU1p_4Opj9HRB7z7J76CE6e_LHcd-KyB48VX1ck44xg5kI4ZePXgphq7DXy2mIDbrtXN5c9Wk9boJYzOaWRDq1JXRoY0U4itG1qTSJ54kSKCQ2ZBeMu0MbqtuVOKnwSJSz6vDZoUpWEmzCX5ZnbBqKkTqOONoFKkW4xa4JQcy06keHaMKV24OhzCWNEs29R6Mzlr0X8vYg7sFXZIZ5UshsxUkuBe3m1-4ev92A59IN6A0FDsQ_zKfqyO4AF-zYdFy-HJUzwPRj2PwBotMgE |
| linkProvider | ProQuest |
| openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Modality-specific+long-term+memory+enhancement+in+Heliconius+butterflies&rft.jtitle=Philosophical+transactions+of+the+Royal+Society+of+London.+Series+B.+Biological+sciences&rft.au=Hodge%2C+Elizabeth+A&rft.au=Alcalde+Anton%2C+Amaia&rft.au=Bestea%2C+Louise&rft.au=Hern%C3%A1ndez%2C+Greta&rft.date=2025-06-26&rft.issn=1471-2970&rft.eissn=1471-2970&rft.volume=380&rft.issue=1929&rft.spage=20240119&rft_id=info:doi/10.1098%2Frstb.2024.0119&rft.externalDBID=NO_FULL_TEXT |
| thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1471-2970&client=summon |
| thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1471-2970&client=summon |
| thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1471-2970&client=summon |