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 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.

Effects of overwintering on the transcriptome and fitness traits in a damselfly with variable voltinism across two latitudes

“…Apart from survival, our results aligned with previous findings in I. elegans , where faster growth rate and reduced development time, as found in the non-winter cohort or when density of individual increases, often come at a cost of having a smaller mass 28 , 33 , 51 . However, previous studies tended to observe the opposite patterns with a smaller size in diapausing individuals 5 , 18 , 19 .…”

“…Our results also showed that the effects of wintering on life-history was mostly independent of the latitude, as none of our variables, except GRM, exhibited significant latitude × wintering interaction. The two latitudes differed significantly in all traits measured with faster growth and lower mass in central-latitude individuals compared to high-latitude individuals, in line with previous studies 15 , 28 . In general, the differences observed between latitudes in the non-winter cohort remained after winter diapause.…”

“…one or two generations per year 16 , 27 . Larvae show large variation in size throughout the growth season and during wintering 16 , 28 with larval head width values, a proxy for larval structural body size and instar, to about 3.5 mm, which corresponds to the final instar prior emergence. Although overwintering was reported at final minus one (F-1) and final instar (F-0) before emergence in northern and central Europe 16 , in univoltine individuals there is a tendency for overwintering in final minus two (F-2) or earlier instars (head width < 2.5 mm) 29 .…”

“…We created a custom Gene Ontology (GO) annotation as described in 28 . For each locus in the I. elegans genome, we retrieved the function and description from NCBI ( https://www.ncbi.nlm.nih.gov/search/all/?term=ischnura%20elegans ).…”

The genomic response to urbanization in the damselfly Ischnura elegans

“…Accumulating evidence suggests that these two life stages are not independent: environmental stressors experienced during the larval stage may affect the cross‐metamorphic adult stage (Sniegula et al, 2020), and stress during the adult stage may carry over to the offspring larval stage (Rolff, 1999). The species has been the subject of intense evolutionary ecological studies on plasticity and adaptive response in the context of climate change, including evolutionary trade‐offs (Stoks & De, 2011; Wos et al, 2023), thermal adaptation (Lancaster et al, 2015, 2016; Shama et al, 2011; Tüzün & Stoks, 2022), and adaptation along environmental gradients (Dudaniec et al, 2018, 2022; Janssens et al, 2014; Raczyński et al, 2022), including urbanization (Solimini et al, 1997). As a generalist species, I. elegans represents a relatively tolerant damselfly when it comes to stressors caused by urbanization (Goertzen & Suhling, 2013; Verheyen et al, 2019; Villalobos‐Jimenez et al, 2016).…”