Academic journal article Genetics

The Genetics of Mating Song Evolution Underlying Rapid Speciation: Linking Quantitative Variation to Candidate Genes for Behavioral Isolation

Academic journal article Genetics

The Genetics of Mating Song Evolution Underlying Rapid Speciation: Linking Quantitative Variation to Candidate Genes for Behavioral Isolation

Article excerpt

SPECIATION can arise from divergence in reproductive phenotypes (Coyne and Orr 2004). Divergent mating behaviors can result in reproductive barriers by causing assortative mating within incipient species. It is well documented that mating behaviors and morphologies diverge early in the speciation process, suggesting an explanation for why prezygotic barriers evolve sooner than postzygotic barriers in the origin of species (e.g., Mendelson 2003; SánchezGuillén et al. 2014). Moreover, some of the most rapid speciation rates known, such as those in Lake Victoria cichlid fish (Seehausen et al. 2008), Hawaiian Laupala crickets (Mendelson and Shaw 2005), Baltic Sea European flounders (Momigliano et al. 2017), and a putative case in Galapagos finches (Lamichhaney et al. 2018), occur when species diverge in mating behaviors and associated structures. Thus, studying the genetics and evolution ofbehavioral barriers can contribute to an emerging general principle of speciation.

Because evolution is a genetic process, characterizing the genetic architecture and identifying genes involved in behavioral barriers is crucial to understanding targets of selection and establishing causal links among genes, pathways, and mating behaviors in the early stages of speciation. In animals, however, courtship is often complex and multimodal, involving many traits (e.g., Greenspan and Ferveur 2000; Rundus et al. 2010; Starnberger et al. 2014; Ullrich et al. 2016; Mowles et al. 2017). Accordingly, it can be difficult to isolate specific behaviors for genetic analysis. Perhaps because of these complexities, we have a limited understanding of the evolutionary genetics of mating behaviors that contribute to reproductive barriers despite its general importance in speciation.

While some progress has been made in understanding the genetic basis of natural variation in visual and olfactory signals, such as cuticular hydrocarbons, sex pheromones, and body coloration [e.g., Gleason et al. 2005, 2009; Kronforst et al. 2006; Sæ ther et al. 2007; Lassance et al. 2010, 2013; Merrill et al 2011; Niehuis et al. 2011; Bay et al. 2017; also reviewed by Groot et al. (2016)], many organisms use acoustic signals involving rhythmic neuromuscular behaviors for which we still have a very limited genetic understanding. Even in Drosophila, where acoustic behavior is expressed widely in courtship, we lack a gene-based understanding of natural variation (but see Gleason and Ritchie 2004; Ding et al 2016). Rhythmic, temporal patterns of such mating "songs" are often species-specific and known components of reproductive barriers among species of insects, fish and amphibians (Gerhardt and Huber 2002; Hartbauer and Römer 2016; Barkan et al. 2017; Smith et al. 2018). The rhythmic elements of song are a result of regularly patterned motor output, products of localized, neural circuits called central pattern generators (CPGs; Chagnaud and Bass 2014; Katz 2016; Schöneich and Hedwig 2017). Compared with other rhythmic mating behaviors such as courtship dance, song rhythms are easy to isolate and measure.

To date, genetic studies of song rhythm variation have revealed a polygenic genetic architecture in insects, including fruit flies, lacewings, crickets, grasshoppers, and moths (Shaw 1996; Williams et al. 2001; Henry et al. 2002; Gleason and Ritchie 2004; Saldamando et al. 2005; Shaw et al. 2007; Ellison et al. 2011; Limousin et al. 2012). However, the causal genes underlying natural variation remain elusive in most cases. Eleven candidate genes that regulate interpulse interval in Drosophila melanogaster, including ion channel genes, transcription factors, and transcription/translation regulators, have been identified through experimentally generated mutations [reviewed by Gleason (2005), also see Turner etal. (2013) and Fedotov etal. (2014, 2018)]. These discoveries offer insight into the types of genes capable of modulating song rhythmicity in naturally occurring systems and thus are reasonable candidate genes for interspecific variation in other singing insects. …

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