The effect of temperature and invasive alien predator on genetic and phenotypic variation in the damselfly Ischnura elegans: cross-latitude comparison

Abstract Background Understanding and predicting how organisms respond to human-caused environmental changes has become a major concern in conservation biology. Here, we linked gene expression and phenotypic data to identify candidate genes underlying existing phenotypic trait differentiation under...

Full description

Bibliographic Details
Main Authors: Guillaume Wos, Gemma Palomar, Marzena Marszałek, Wiesław Babik, Szymon Sniegula
Format: Article
Language:English
Published: BMC 2023-04-01
Series:Frontiers in Zoology
Subjects:
Online Access:https://doi.org/10.1186/s12983-023-00494-z
_version_ 1797845787300855808
author Guillaume Wos
Gemma Palomar
Marzena Marszałek
Wiesław Babik
Szymon Sniegula
author_facet Guillaume Wos
Gemma Palomar
Marzena Marszałek
Wiesław Babik
Szymon Sniegula
author_sort Guillaume Wos
collection DOAJ
description Abstract Background Understanding and predicting how organisms respond to human-caused environmental changes has become a major concern in conservation biology. Here, we linked gene expression and phenotypic data to identify candidate genes underlying existing phenotypic trait differentiation under individual and combined environmental variables. For this purpose, we used the damselfly Ischnura elegans. Egg clutches from replicated high- (southern Sweden) and central-latitude (southern Poland) populations facing different degrees of seasonal time constraints were collected. Damselfly larvae were exposed to experimental treatments: current and mild warming temperatures crossed with the presence or absence of an invasive alien predator cue released by the spiny-cheek crayfish, Faxonius limosus, which is only present in Poland to date. We measured the following traits: larval development time, body size, mass and growth rate, and used the larvae for gene expression analysis by RNA-seq. Data were analysed using a multivariate approach. Results We showed latitudinal differences in coping with mild warming and predator cues. When exposed to an increased temperature and a predator cue, central-latitude individuals had the shortest development and the fastest growth compared to high-latitude individuals. There was a general effect of predator cues regarding mass and growth rate reduction independent of latitude. Transcriptome analysis revealed that metabolic pathways related to larval anatomy and development tended to be upregulated in response to mild warming but only in fast-growing central-latitude individuals. Metabolic pathways linked to oxidative stress tended to be downregulated in response to a predator cue, especially in central-latitude individuals. Conclusion Different phenotypic and transcriptomic responses to environmental factors might be attributed to the variability in I. elegans life history strategies between the two latitudes caused by seasonal time constraints and to its coexistence with the invasive alien predator in nature. By providing insights into how organisms may respond to future anthropogenic changes, our results may be of particular interest in conservation biology.
first_indexed 2024-04-09T17:45:39Z
format Article
id doaj.art-08eb088b933340978360ce87aeff08d7
institution Directory Open Access Journal
issn 1742-9994
language English
last_indexed 2024-04-09T17:45:39Z
publishDate 2023-04-01
publisher BMC
record_format Article
series Frontiers in Zoology
spelling doaj.art-08eb088b933340978360ce87aeff08d72023-04-16T11:20:41ZengBMCFrontiers in Zoology1742-99942023-04-0120111410.1186/s12983-023-00494-zThe effect of temperature and invasive alien predator on genetic and phenotypic variation in the damselfly Ischnura elegans: cross-latitude comparisonGuillaume Wos0Gemma Palomar1Marzena Marszałek2Wiesław Babik3Szymon Sniegula4Institute of Nature Conservation Polish Academy of SciencesInstitute of Nature Conservation Polish Academy of SciencesInstitute of Environmental Sciences, Jagiellonian UniversityInstitute of Environmental Sciences, Jagiellonian UniversityInstitute of Nature Conservation Polish Academy of SciencesAbstract Background Understanding and predicting how organisms respond to human-caused environmental changes has become a major concern in conservation biology. Here, we linked gene expression and phenotypic data to identify candidate genes underlying existing phenotypic trait differentiation under individual and combined environmental variables. For this purpose, we used the damselfly Ischnura elegans. Egg clutches from replicated high- (southern Sweden) and central-latitude (southern Poland) populations facing different degrees of seasonal time constraints were collected. Damselfly larvae were exposed to experimental treatments: current and mild warming temperatures crossed with the presence or absence of an invasive alien predator cue released by the spiny-cheek crayfish, Faxonius limosus, which is only present in Poland to date. We measured the following traits: larval development time, body size, mass and growth rate, and used the larvae for gene expression analysis by RNA-seq. Data were analysed using a multivariate approach. Results We showed latitudinal differences in coping with mild warming and predator cues. When exposed to an increased temperature and a predator cue, central-latitude individuals had the shortest development and the fastest growth compared to high-latitude individuals. There was a general effect of predator cues regarding mass and growth rate reduction independent of latitude. Transcriptome analysis revealed that metabolic pathways related to larval anatomy and development tended to be upregulated in response to mild warming but only in fast-growing central-latitude individuals. Metabolic pathways linked to oxidative stress tended to be downregulated in response to a predator cue, especially in central-latitude individuals. Conclusion Different phenotypic and transcriptomic responses to environmental factors might be attributed to the variability in I. elegans life history strategies between the two latitudes caused by seasonal time constraints and to its coexistence with the invasive alien predator in nature. By providing insights into how organisms may respond to future anthropogenic changes, our results may be of particular interest in conservation biology.https://doi.org/10.1186/s12983-023-00494-zGene expression analysisGlobal changesHuman disturbanceInvasive alien speciesIschnura elegansLatitude
spellingShingle Guillaume Wos
Gemma Palomar
Marzena Marszałek
Wiesław Babik
Szymon Sniegula
The effect of temperature and invasive alien predator on genetic and phenotypic variation in the damselfly Ischnura elegans: cross-latitude comparison
Frontiers in Zoology
Gene expression analysis
Global changes
Human disturbance
Invasive alien species
Ischnura elegans
Latitude
title The effect of temperature and invasive alien predator on genetic and phenotypic variation in the damselfly Ischnura elegans: cross-latitude comparison
title_full The effect of temperature and invasive alien predator on genetic and phenotypic variation in the damselfly Ischnura elegans: cross-latitude comparison
title_fullStr The effect of temperature and invasive alien predator on genetic and phenotypic variation in the damselfly Ischnura elegans: cross-latitude comparison
title_full_unstemmed The effect of temperature and invasive alien predator on genetic and phenotypic variation in the damselfly Ischnura elegans: cross-latitude comparison
title_short The effect of temperature and invasive alien predator on genetic and phenotypic variation in the damselfly Ischnura elegans: cross-latitude comparison
title_sort effect of temperature and invasive alien predator on genetic and phenotypic variation in the damselfly ischnura elegans cross latitude comparison
topic Gene expression analysis
Global changes
Human disturbance
Invasive alien species
Ischnura elegans
Latitude
url https://doi.org/10.1186/s12983-023-00494-z
work_keys_str_mv AT guillaumewos theeffectoftemperatureandinvasivealienpredatorongeneticandphenotypicvariationinthedamselflyischnuraeleganscrosslatitudecomparison
AT gemmapalomar theeffectoftemperatureandinvasivealienpredatorongeneticandphenotypicvariationinthedamselflyischnuraeleganscrosslatitudecomparison
AT marzenamarszałek theeffectoftemperatureandinvasivealienpredatorongeneticandphenotypicvariationinthedamselflyischnuraeleganscrosslatitudecomparison
AT wiesławbabik theeffectoftemperatureandinvasivealienpredatorongeneticandphenotypicvariationinthedamselflyischnuraeleganscrosslatitudecomparison
AT szymonsniegula theeffectoftemperatureandinvasivealienpredatorongeneticandphenotypicvariationinthedamselflyischnuraeleganscrosslatitudecomparison
AT guillaumewos effectoftemperatureandinvasivealienpredatorongeneticandphenotypicvariationinthedamselflyischnuraeleganscrosslatitudecomparison
AT gemmapalomar effectoftemperatureandinvasivealienpredatorongeneticandphenotypicvariationinthedamselflyischnuraeleganscrosslatitudecomparison
AT marzenamarszałek effectoftemperatureandinvasivealienpredatorongeneticandphenotypicvariationinthedamselflyischnuraeleganscrosslatitudecomparison
AT wiesławbabik effectoftemperatureandinvasivealienpredatorongeneticandphenotypicvariationinthedamselflyischnuraeleganscrosslatitudecomparison
AT szymonsniegula effectoftemperatureandinvasivealienpredatorongeneticandphenotypicvariationinthedamselflyischnuraeleganscrosslatitudecomparison