Genome Structure and Signatures of Cold Specialization in Beetles
Despite many attempts to find abiotic and biotic factors that contribute to the enormous natural variation in genome size, it remains an open question which evolutionary and ecological variables drive genome size changes (Blommaert 2020). The main challenges to resolving this question arise from the complexity of genome composition, decoupling the role of selection (if present) from many different environmental factors, and the dependence of genome size on phylogenetic relatedness (Alfsneset al. 2017; Canapa et al. 2020; Ritchie et al.2017). Recent studies have shown that the genome size is positively correlated with the size of repetitive DNA in insects (Quesneville 2015), but repetitive DNA has been linked to both adaptive and non-adaptive evolutionary processes (Canapa et al. 2015; Loweret al. 2017). To date, there has been limited effort to document evidence for a statistical association between genome size and environmental factors in insects (Alfsnes et al. 2017). One exception involves the Antarctic midge, Belgica antarctica, which is endemic to Antarctica and has (to date) the smallest genome of any insect species (99 MB), and very little TE content in the genome (Kelleyet al. 2014). In concordance with the case of B. antarctica , we show that the cold-adapted alpine ground beetle N. riversi has the smallest assembled genome among sequenced beetles, including eight species of Adephaga and 11 species of Polyphaga (Table S6 ). This is associated with a smaller size range of introns and less TE content (Table 1 ), and may support the hypothesis that smaller genomes are associated with adaptation to extreme environments such as polar or alpine climates (Kelley et al. 2014). A possible adaptive driver of this pattern is that smaller genome size results in bioenergetic savings (Wagner 2005; Wrightet al. 2014), such as a more efficient cell cycling, transcription and metabolism, allowing species to develop faster and maximize the efficiency of cellular processes. Such changes might compensate for the relatively shorter growth season in the cold environments, as well as the fact that low temperatures elongate cell cycle duration and slow cellular metabolism in ectotherms (Vinogradov 1999). However, the relationship between genome size and cold temperature is reversed in crustaceans and many vertebrates (Canapaet al. 2020), posing something of a conundrum. Other cold-specialized insects also defy this pattern, such as the alpine grasshopper Gomphocerus sibiricus , which has a spectacularly large 8.95 Gb genome (Gosalvez et al. 1980). Some have argued that different strategies might be employed depending on the developmental biology of organisms (Alfsnes et al. 2017). In insects, previous research has shown that holometabolous insects (with complete metamorphosis) have smaller genomes than hemimetabolous insects (Alfsnes et al. 2017), suggesting that the complex developmental changes in metamorphosis are an added factor constraining genome size. Clearly, more comparative genomics research, preferably sampling variable genome sizes among more closely related taxa, is needed to test these hypotheses.