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.