Timing strains of the marine insect Clunio marinus diverged and persist with gene flow

Abstract

Genetic divergence of populations in the presence of gene flow is a central theme in speciation research. Theory predicts that divergence can happen with full range overlap – in sympatry – driven by ecological factors, but there are few empirical examples of how ecologically divergent selection can overcome gene flow and lead to reproductive isolation. In the marine midge Clunio marinus (Diptera: Chironomidae) reproduction is ecologically restricted to the time of the lowest tides, which is ensured through accurate control of development and adult emergence by circalunar and circadian clocks. As tidal regimes differ along the coastline, locally adapted timing strains of C. marinus are found in different sites across Europe. At the same time, ecologically suitable low tides occur at both full and new moon and twice a day, providing C. marinus with four nonoverlapping temporal niches at every geographic location. Along the coast of Brittany, which is characterized by a steep gradient in timing of the tides, we found an unusually large number of differentially adapted timing strains, and the first known instances of sympatric C. marinus strains occupying divergent temporal niches. Analysis of mitochondrial genotypes suggests that these timing strains originated from a single recent colonization event. Nuclear genotypes show strong gene flow, sympatric timing strains being the least differentiated. Even when sympatric strains exist in nonoverlapping temporal niches, timing adaptations do not result in genome‐wide genetic divergence, suggesting timing adaptations are maintained by permanent ecological selection. This constitutes a model case for incipient ecological divergence with gene flow.

An oligogenic architecture underlying ecological and reproductive divergence in sympatric populations

“…In the F2 ( D ), the phenotypes spread out again, but do not segregate completely, suggesting that more than one locus controls lunar emergence time. The peaks around day 20 (grey shading) are direct responses to the artificial moonlight treatment (see 21 ). They do not occur in the field and were not considered in our analyses.…”

“…Notably, full moon and new moon low tides are ecologically equally suitable for C. marinus’ reproduction, representing different timing niches that are occupied by different timing types (for details and definitions see 21 ). Some timing types of C. marinus use both niches ( “ s emilunar rhythm” ; SL type), but there are also dedicated full moon (FM) or new moon (NM) timing types, which occupy only one timing niche 21 . Divergence into FM and NM timing types represents a magic trait, as it automatically entails assortative mating.…”

Hybridization Dynamics and Extensive Introgression in theDaphnia longispinaSpecies Complex: New Insights from a High-QualityDaphnia galeataReference Genome

“…The hybrid breakdown observed in this system reduces the likelihood of introgression via backcrossing. On the other side of the spectrum, hybridization is followed by introgression, and ongoing exchange of genetic information between species ( Martin et al 2013 ; Butlin et al 2014 ; Doellman et al 2018 ; Kaiser et al 2021 ). Several empirical studies ( Canestrelli et al 2017 ; Schreiber and Pfenninger 2021 ) as well as theoretical models ( Yeaman and Whitlock 2011 ; Flaxman et al 2014 ; Rafajlović et al 2016 ) suggest the possibility of intermediate constant equilibrium states, meaning that certain parts of the genome remain diverged (islands or continents of divergence), whereas others are freely exchanged among closely related species without ever reaching complete genomic isolation.…”

On the fitness of informative cues in complex environments

“…Clunio is adapted to one of the most complex environments on earth, the intertidal zone of seacoasts. Synchronizing the adult emergence time to multiple environmental cycles of tidal, diurnal and lunar cycles, the marine midge has successfully adapted in processing complex informative cues [45,46,47]. Using cues, adults emerge In conclusion, we have extended the study of bet-hedging to asymmetric cases where phenotypes are scarcer than the number of different environmental states.…”