An oligogenic architecture underlying ecological and reproductive divergence in sympatric populations
Curation statements for this article:-
Curated by eLife
eLife assessment
This potentially important article identifies an apparent oligogenic architecture for an ecologically relevant trait, the circalunar reproduction of marine midges, which contributes to assortative mating, is likely under divergent selection, and supports reproductive isolation in sympathy. A claim for a causal role of chromosomal inversions in this system is made, but the support for this claim is incomplete.
This article has been Reviewed by the following groups
Listed in
- Evaluated articles (eLife)
- Evolutionary Biology (eLife)
Abstract
The evolutionary trajectories and genetic architectures underlying ecological divergence with gene flow are poorly understood. Sympatric timing types of the intertidal insect Clunio marinus (Diptera) from Roscoff (France) differ in lunar reproductive timing. One type reproduces at full moon, the other at new moon, controlled by a circalunar clock of yet unknown molecular nature. Lunar reproductive timing is a magic trait for a sympatric speciation process, as it is both ecologically relevant and entails assortative mating. Here, we show that the difference in reproductive timing is controlled by at least four quantitative trait loci (QTL) on three different chromosomes. They are partly associated with complex inversions, but differentiation of the inversion haplotypes cannot explain the different phenotypes. The most differentiated locus in the entire genome, with QTL support, is the period locus, implying that this gene could not only be involved in circadian timing but also in lunar timing. Our data indicate that magic traits can be based on an oligogenic architecture and can be maintained by selection on several unlinked loci.
Article activity feed
-
-
eLife assessment
This potentially important article identifies an apparent oligogenic architecture for an ecologically relevant trait, the circalunar reproduction of marine midges, which contributes to assortative mating, is likely under divergent selection, and supports reproductive isolation in sympathy. A claim for a causal role of chromosomal inversions in this system is made, but the support for this claim is incomplete.
-
Reviewer #1 (Public Review):
Several new observations on the fascinating marine midge system are provided. The results are robust and have broad interest. First, multiple polymorphic chromosomal inversions are shown to be segregating in the study populations but these inversions are not strongly associated with ecotype differentiation. At least 4 QTL are detected that together explain a large part of the timing difference between co-located populations that emerge at full and new moon. Good candidate genes under these QTL are identified, with unusually high differentiation between populations. These are involved in the circadian clock (period) and in nervous system rewiring. The involvement of period suggests a link between the circadian and circalunar clocks.
The major context provided by the authors is the idea of 'magic traits' that …
Reviewer #1 (Public Review):
Several new observations on the fascinating marine midge system are provided. The results are robust and have broad interest. First, multiple polymorphic chromosomal inversions are shown to be segregating in the study populations but these inversions are not strongly associated with ecotype differentiation. At least 4 QTL are detected that together explain a large part of the timing difference between co-located populations that emerge at full and new moon. Good candidate genes under these QTL are identified, with unusually high differentiation between populations. These are involved in the circadian clock (period) and in nervous system rewiring. The involvement of period suggests a link between the circadian and circalunar clocks.
The major context provided by the authors is the idea of 'magic traits' that influence multiple components of reproductive isolation and so are potentially important in population differentiation because associations between traits do not need to be built and maintained in the face of recombination. This idea is not described very clearly in the current MS. In particular, the authors suggest that magic traits are expected to have simple genetic basis, an expectation that they say should be re-evaluated on the basis of their results. However, there is no strong justification for this expectation. It tends to confuse the magic trait idea with the possibility of pleiotropy and with the advantage of recombination suppression where local adaptation is opposed by gene flow. The latter is relevant here because of the involvement of inversions, which might be expected to capture multiple alleles contributing to local adaptation but here apparently do not do so.
-
Reviewer #2 (Public Review):
Briševac et al. investigate the genetic architecture of an exceptional ecological system where Clunio marinus populations have diverged in their timing of reproduction, controlled by a circalunar clock. These loci may be important in sympatric speciation and/or rapid evolution of reproductive isolation but there are some issues that need to be resolved. I outline these below:
The QTL mapping relies on a modest number of individuals and there are important details missing. The manuscript is missing information on heritability of the trait which is important for interpretation. While the variance explained by the QTL is hight, for the estimates of QTL effect sizes from such small samples, there is a common issue known as the Beavis effect that can inflate the effect size of individual QTL.
My major concern with …
Reviewer #2 (Public Review):
Briševac et al. investigate the genetic architecture of an exceptional ecological system where Clunio marinus populations have diverged in their timing of reproduction, controlled by a circalunar clock. These loci may be important in sympatric speciation and/or rapid evolution of reproductive isolation but there are some issues that need to be resolved. I outline these below:
The QTL mapping relies on a modest number of individuals and there are important details missing. The manuscript is missing information on heritability of the trait which is important for interpretation. While the variance explained by the QTL is hight, for the estimates of QTL effect sizes from such small samples, there is a common issue known as the Beavis effect that can inflate the effect size of individual QTL.
My major concern with the paper is the interpretation of divergence within the inversion as linked causally to the genes underlying ecological divergence. As the authors observe, divergence will vary within an inverted region. This can be traced to myriad factors, including variation in mutation rate, variation in constraint, patterns of ancestral polymorphism within this region, and variation in gene conversion within the inversion. Given this, I do not think it is valid to interpret the regions of high differentiation as the causal drivers of the ecological differentiation.
The authors imply in the discussion based on historical results that the ecotype evolved in situ in the last ~60 years. This seems substantially less likely to me than a number of alternative hypotheses including missing the phenotype in previous samples, plasticity in the phenotype causing it to be missed or migration from populations where the phenotype already existed.
-
-