Multiple genetic loci affect place learning and memory performance in Drosophila melanogaster

Abstract

Learning and memory are critical functions for all animals, giving individuals the ability to respond to changes in their environment. Within populations, individuals vary, however the mechanisms underlying this variation in performance are largely unknown. Thus, it remains to be determined what genetic factors cause an individual to have high learning ability and what factors determine how well an individual will remember what they have learned. To genetically dissect learning and memory performance, we used the Drosophila synthetic population resource (DSPR), a multiparent mapping resource in the model system Drosophila melanogaster, consisting of a large set of recombinant inbred lines (RILs) that naturally vary in these and othertraits. Fruit flies can be trained in a "heat box" to learn to remain on one side of a chamber (place learning) and can remember this (place memory) over short timescales. Using this paradigm, we measured place learning and memory for~49 000 individual flies from over 700 DSPR RILs. We identified 16 different loci across the genome that significantly affect place learning and/or memory performance, with 5 of these loci affecting both traits. To identify transcriptomic differences associated with performance, we performed RNA-Seq on pooled samples of seven high performing and seven low performing RILs for both learning and memory and identified hundreds of genes with differences in expression in the two sets. Integrating our transcriptomic results with the mapping results allowed us to identify nine promising candidate genes, advancing our understanding of the genetic basis underlying natural variation in learning and memory performance.K E Y W O R D S differential gene expression, Drosophila melanogaster, learning, memory, multiparental population, QTL

Genome annotation with long RNA reads reveals new patterns of gene expression and improves single-cell analyses in an ant brain

“…S5E), suggesting potential co-regulation of the coding and noncoding transcript in cis as previously reported for other lncRNAs-mRNA pairs [ 58 ]. Drosophila wdp encodes a transmembrane protein with known functions in the wing disc [ 59 ] and the trachea [ 60 ], and it has also been implicated in synaptic target recognition [ 61 ] and learning [ 62 ]. While the sequence of the lncRNA LOC112590028 itself is not conserved, Drosophila has a lncRNA, CR44758 in the same position as LOC112590028, between wdp and Gp150 (Fig.…”

The Evolutionary Relevance of Social Learning and Transmission in Non-Social Arthropods with a Focus on Oviposition-Related Behaviors

“…There is evidence that most behaviors and behavioral variation between individuals have some genetic basis [49][50][51][52][53]. For example, several candidate loci were identified and associated with phenotypic variation for memorizing locations in the fly Drosophila melanogaster [54]. The identification of candidate loci paves the way for finding the genetic basis of complex behavioral traits, including spatial exploration ability and memory retention of spatial location (e.g., of suitable resources, including host plants for oviposition).…”

“…Genetic variants with higher learning capacity and memory retention may thus become more numerous in successive generations, when there is positive selection for oviposition site selection (Figure 2). There is further evidence that learning ability itself has a genetic basis and that there is genetic variation in learning ability between individuals in various invertebrate, non-social taxa (reviewed in [54][55][56][57][58]). One gene whose allelic variation and expression is associated with differential learning rate and memory retention is the foraging gene ("for"), a pleiotropic gene that produces a cyclic GMP-dependent protein kinase (PKG), a protein involved in many regulatory functions, including energy homeostasis [59][60][61][62].…”

The evolutionary relevance of social learning and transmission of behaviors in non-social arthropods

“…There is evidence that most behaviors and behavioral variation between individuals have some genetic basis [37][38][39][40][41]. For example, several candidate loci were identified and associated with phenotypic variation for memorizing locations in the fly Drosophila melanogaster [42]. The identification of candidate loci paves the way for finding the genetic basis of complex behavioral traits, including spatial exploration ability (e.g., spatial learning rate) and memory retention of spatial location (e.g., suitable resources, including host plants for oviposition).…”

“…Genetic variants with higher learning rate and memory retention may thus become more numerous in successive generations, when there is positive selection for oviposition site selection (Figure 2). There is further evidence that learning ability itself has a genetic basis and that there is genetic variation in learning ability between individuals in various invertebrate, non-social taxa (reviewed in [42][43][44][45][46]). One gene whose allelic variation and expression is associated with differential learning rate and memory retention is the foraging gene ("for"), a pleiotropic gene that produces a cyclic GMP-dependent protein kinase (PKG), the protein of which is involved in energy homeostasis [47][48][49][50].…”