Sex chromosomes and chromosomal rearrangements are key to behavioural sexual isolation in Jaera albifrons marine isopods
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Abstract
The lack of sexual attraction between individuals from different populations is a direct barrier to gene flow between these populations. Here we focus on the evolution of this class of isolating mechanism, behavioural sexual isolation, through the empirical study of two closely related species of small marine isopods. The males of Jaera albifrons and J. praehirsuta similarly engage females in tactile courtship by brushing a specific region of the female's back, but they do so with divergent sets of specialised setae and spines, and female choice results in strong reproductive isolation. Using bi-allelic SNP genotypes obtained from double-digest RAD sequencing of individuals from natural populations and controlled crosses, we found that secondary contacts between J. albifrons and J. praehirsuta resulted in different levels of heterospecific gene flow depending on the ecological context. Comparison of the genomic landscapes of differentiation in the two most contrasting situations (extremely low heterospecific gene flow in one region of western France, but strong introgressive hybridisation in another), combined with linkage map analyses, allowed us to conclude that genomic regions impervious to interspecies gene flow are primarily located either on the sex chromosomes or on rearranged chromosomes (several fusion-scissions and one reciprocal translocation). These genomic regions show low recombination, and in two cases QTL analyses found genetic variation associated with several male courtship traits. These results suggest that a long period of allopatry may have allowed the divergent co-evolution of male traits and female preferences, with genetic bases located at least in part in non-recombining regions on sex chromosomes and rearranged chromosomes.
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The cause of isolation between species is often very difficult to determine, because multiple phenomena and layers usually come together in a given situation. Different species can live in different habitats, which limits their opportunity to meet (ecological premating isolation). They can also exhibit different sexual traits and preferences, which limit their opportunity to mate (sexual premating isolation). Furthermore, their offspring can suffer from lower viability and fertility, which limits further genetic exchanges (postmating isolation). The genetic basis of these phenomena has been under scrutiny for decades, but when ecology matters, depends on difficult field studies in a few model systems.
In the 1950s–1970s, the intertidal marine isopods from the Jaera albifrons complex were a useful model for systematicians and …
The cause of isolation between species is often very difficult to determine, because multiple phenomena and layers usually come together in a given situation. Different species can live in different habitats, which limits their opportunity to meet (ecological premating isolation). They can also exhibit different sexual traits and preferences, which limit their opportunity to mate (sexual premating isolation). Furthermore, their offspring can suffer from lower viability and fertility, which limits further genetic exchanges (postmating isolation). The genetic basis of these phenomena has been under scrutiny for decades, but when ecology matters, depends on difficult field studies in a few model systems.
In the 1950s–1970s, the intertidal marine isopods from the Jaera albifrons complex were a useful model for systematicians and cytogeneticists studying speciation and the role of chromosomal rearrangements (1–3). J. albifrons and J. praehirsuta, two species of that complex, are characterised by ecological and sexual isolation, but little postzygotic isolation, as can be concluded from the limited number of laboratory cross-breeding experiments conducted (4). In the field, however, these species sometimes share the same pebble habitat (notably in Normandy), while at other times they live in different algal versus pebble habitats (notably in Brittany). This system therefore allows contrasting two interesting situations in which both ecological and sexual premating isolation occur between the two species in Brittany, while only sexual premating isolation occurs in Normandy. Could this contrast reveal the contribution of ecological versus sexual isolation mechanisms? Can it reveal the genetic basis of sexual isolation? Can it reveal the role of chromosomal rearrangements in these contrasted cases?
In this study, Ambre Ribardière and colleagues embark on this comparison using a remarkable variety of genomic approaches, careful analyses and extensive data. Their first major finding is that genomic differentiation between species indeed is lower when only sexual isolation is operating than when both ecological and sexual isolation are operating. Second, they found that this differentiation is highly heterogeneous across the genome with only a subset of regions found highly differentiated in Normandy compared to Brittany. Third, most of these regions involve regions with low recombination, notably on sex chromosomes, but also on a few rearranged autosomes. Fourth, QTL loci for male sexual traits colocalise in these regions.With these findings, they demonstrate elegantly that in the absence of ecological isolation, many genomic regions become homogenized by gene flow, while some regions resist its eroding effect, being likely involved in sexual isolation. This study also prompts new questions: what explains the important role of sex chromosomes in this context? The large X/Z effect is usually understood in the context of post-mating, not sexual, isolation (5, 6). Is there absolutely no post-mating isolation in these hybrids, with some Haldane rule pattern? Is the overrepresentation of low recombination regions merely a consequence of QTL detection bias? Are there other field locations where different or parallel contrasts can be made? Undoubtedly, however, with this landmark study, the Jaera albifrons complex (re)emerges as a new and fascinating model system for speciation research in the genomic era.
References
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2. P. Lecher, Cytogénétique de l’hybridisation expérimentale et naturelle chez l’isopode Jaera (albifrons) syei Bocquet. Archives de Zoologie Expérimentale et Générale 108, 633–698 (1967).
3. M. Solignac, Isolating mechanisms and modalities of speciation in the Jaera albifrons species complex (Crustacea, Isopoda). Syst. Zool. 30, 387–405 (1981). https://doi.org/10.1093/sysbio/30.4.387
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5. A. Ribardière, C. Daguin-Thiébaut, J. Coudret, G. Le Corguillé, K. Avia, C. Houbin, S. Loisel, P.-A. Gagnaire, T. Broquet. Sex chromosomes and chromosomal rearrangements are key to behavioural sexual isolation in Jaera albifrons marine isopods. bioRxiv, ver.3 (2025) peer-reviewed and recommended by PCI Evolutionary Biology. https://doi.org/10.1101/2025.01.08.631900
6. J. A. Coyne, H. A. Orr, “Two rules of speciation” in Speciation and Its Consequences (Sinauer, Sunderland, MA, D Otte; J Endler., 1989), pp. 180–207.
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