Abstract
Understanding the processes of adaptive divergence, which may ultimately lead to speciation, is a major question in evolutionary biology. Allochronic differentiation refers to a particular situation where gene flow is primarily impeded by temporal isolation between early and late reproducers. This process has been suggested to occur in a large array of organisms, even though it is still overlooked in the literature. We here focused on a well-documented case of incipient allochronic speciation in the winter pine processionary moth Thaumetopoea pityocampa. This species typically reproduces in summer and larval development occurs throughout autumn and winter. A unique, phenologically shifted population (SP) was discovered in 1997 in Portugal. It was proved to be strongly differentiated from the sympatric "winter population" (WP), but its evolutionary history could only now be explored. We took advantage of the recent assembly of a draft genome and of the development of pan-genomic RAD-seq markers to decipher the demographic history of the differentiating populations and develop genome scans of adaptive differentiation. We showed that the SP diverged relatively recently, that is, few hundred years ago, and went through two successive bottlenecks followed by population size expansions, while the sympatric WP is currently experiencing a population decline. We identified outlier SNPs that were mapped onto the genome, but none were associated with the phenological shift or with subsequent adaptations. The strong genetic drift that occurred along the SP lineage certainly challenged our capacity to reveal functionally important loci.
Highlights
Ecological speciation in sympatry, the process by which adaptation to contrasting ecological conditions drives the divergence of co-occurring populations, has received growing attention in the last 12 years (Rundle & Nosil, 2005)
The first axis of variation (PC1) accounted for 93.5% of the total genetic variation and separated the samples according to the phenology of their underlying population (i.e., LSP1 and LSP2 vs. LWP1, LWP2 and AWP)
The model was significantly improved by including changes in population sizes and migration between populations, suggesting that the demographic history associated with the allochronic event is relatively complex
Summary
Ecological speciation in sympatry, the process by which adaptation to contrasting ecological conditions drives the divergence of co-occurring populations, has received growing attention in the last 12 years (Rundle & Nosil, 2005). Isolation-by-time can further lead to adaptation-by-time (Hendry & Day, 2005) when divergent selection operates between contrasting environmental conditions encountered at the different breeding times This process remains largely unexplored in the literature, but has been suggested to occur in a large array of organisms such as plants (Devaux & Lande, 2008; Savolainen et al, 2006; Weis et al., 2005), birds (Friesen et al, 2007), fishes (Limborg, Waples, Seeb, & Seeb, 2014), corals (Rosser, 2015, 2016) or insects (Santos, Burban, et al, 2011; Sota et al, 2013; Yamamoto & Sota, 2009, 2012; Yamamoto, Beljaev, & Sota, 2016). To go beyond the description of such case studies and disentangle the evolutionary scenarios underlying allochronic differentiation, much remains to be done; in particular, the initial reduction of migration rate between the diverging populations and the underlying genomic mechanisms remain to be explored in most cases
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