Evolutionary dynamics of recent selection for enhanced social cognition

Abstract

Cognitive abilities can vary dramatically among species though little is known about the dynamics of cognitive evolution. Here we demonstrate that recent evolution of visual individual recognition in the paper wasp Polistes fuscatus is the target of arguably the strongest positive selective pressure in the species' recent history. The most extreme selective sweeps in P.fuscatus are associated with genes known to be involved in long-term memory formation, mushroom body development and visual processing -all traits that have recently evolved in association with individual recognition. Cognitive evolution appears to have been driven initially by selection on standing variation in perceptual traits followed by both hard and soft sweeps on learning and memory. Evolutionary modeling reveals that intense selection as observed in P.fuscatus is likely the norm during the early stages of cognitive evolution. These data provide insight into the dynamics of cognition evolution demonstrating that social selection for increased intelligence can lead to rapid multi-genic adaptation of enhanced recognition abilities. Main TextCognition is arguably among the most complex animal traits and has been instrumental in the ecological and evolutionary success of disparate lineages (1). Despite intense interest, the

Identity signaling, identity reception and the evolution of social recognition in a Neotropical frog

“…Our empirical support for the identity reception hypothesis offers an important and rare example of receivers responding to selection in the context of social recognition. Compared to other components of recognition systems, the perceptual and cognitive basis of social recognition is an aspect of receiver psychology [49] that has received less attention and largely remains a "black box" [10,50], but see [11,13,26,47,51]. Indeed, the combination of perception, learning, and memory that collectively constitutes a receiver's "psychological landscape" [49] is often implicitly assumed to be a relatively static feature of nervous systems that acts as a source of selection on signals [50].…”

Expansion and accelerated evolution of 9-exon odorant receptors inPolistespaper wasps

“…Polistes use chemicals as signals and cues in a variety of behaviors, including during mate attraction, mate compatibility recognition, queen recognition, dominance/fertility signaling, and nestmate recognition (Reed & Landolt 1990;Post & Jeanne 1984;Dapporto et al 2007;Jandt et al 2014;Sledge et al 2001aSledge et al , 2001bSledge et al , 2004Oi et al 2019;Espelie et al 1994). Recent efforts to sequence Polistes genomes provide an opportunity to resolve patterns of OR evolution among closely related species as an independent test of 9-exon OR gene subfamily expansion during social evolution and (Patalano et al 2015;Standage et al 2016;Miller SE et al 2020). We annotated the OR repertoires of five Polistes species representing ~40 million years of evolution: P. fuscatus, P. metricus, P. dorsalis, P. canadensis, and P. dominula (Figure 1).…”

“…OR annotation in P. fuscatus: The Polistes fuscatus genome was assembled as described in Miller SE et al 2020 (Robertson et al 2003, Robertson et al 2010, Zhou et al 2012, Zhou et al 2015, Brand & Ramirez 2017, McKenzie & Kronauer 2018. The P. fuscatus genome was queried with amino acid sequences from each of the listed species using the TBLASTN algorithm with an e-value cutoff of 1e-5 (Altschul et al 1997).…”

“…The Polistes dorsalis and Polistes metricus genomes were assembled and annotated as described in Miller SE et al 2020…”

“…Across a sample of insects, the number of intact OR genes in 130 the genome correlates with the number of glomeruli in the antennal lobe, predicting 229 ORs in 131 the P. fuscatus genome ( Figure 2). Here we focus on the P. fuscatus genome because it has nearly 132 chromosome level scaffolds and is the best assembled Polistes genome (Table S1; Patalano et al 133 2015;Standage et al 2016;Miller SE et al 2020). Automated annotation using the MAKER 134 pipeline (Holt & Yandell 2011) without guidance from antennal mRNA predicted 115 OR gene 135 models in the P. fuscatus genome.…”