Pierre R. Gérard

Assortative mating and differential male mating success in an ash hybrid zone population.

BackgroundThe structure and evolution of hybrid zones depend mainly on the relative importance of dispersal and local adaptation, and on the strength of assortative mating. Here, we study the influence of dispersal, temporal isolation, variability in phenotypic traits and parasite attacks on the male mating success of two parental species and hybrids by real-time pollen flow analysis. We focus on a hybrid zone population between the two closely related ash species Fraxinus excelsior L. (common ash) and F. angustifolia Vahl (narrow-leaved ash), which is composed of individuals of the two species and several hybrid types. This population is structured by flowering time: the F. excelsior individuals flower later than the F. angustifolia individuals, and the hybrid types flower in-between. Hybrids are scattered throughout the population, suggesting favorable conditions for their local adaptation. We estimate jointly the best-fitting dispersal kernel, the differences in male fecundity due to variation in phenotypic traits and level of parasite attack, and the strength of assortative mating due to differences in flowering phenology. In addition, we assess the effect of accounting for genotyping error on these estimations.ResultsWe detected a very high pollen immigration rate and a fat-tailed dispersal kernel, counter-balanced by slight phenological assortative mating and short-distance pollen dispersal. Early intermediate flowering hybrids, which had the highest male mating success, showed optimal sex allocation and increased selfing rates. We detected asymmetry of gene flow, with early flowering trees participating more as pollen donors than late flowering trees.ConclusionThis study provides striking evidence that long-distance gene flow alone is not sufficient to counter-act the effects of assortative mating and selfing. Phenological assortative mating and short-distance dispersal can create temporal and spatial structuring that appears to maintain this hybrid population. The asymmetry of gene flow, with higher fertility and increased selfing, can potentially confer a selective advantage to early flowering hybrids in the zone. In the event of climate change, hybridization may provide a means for F. angustifolia to further extend its range at the expense of F. excelsior.

Temporal cline in a hybrid zone population between Fraxinus excelsior L. and Fraxinus angustifolia Vahl

The two closely related ash species Fraxinus excelsior L. (common ash) and Fraxinus angustifolia Vahl (narrow‐leaved ash) have a broad contact zone in France where they hybridize. However, little is known about the local structure of hybrid zone populations and the isolation mechanisms. We assessed the potential effect of floral phenology on the structure of a riparian ash hybrid zone population in central France. The distribution of flowering times was unimodal and lay between the flowering periods of the two species. Using microsatellite markers, we detected isolation by time, which has possibly originated from assortative mating. Multivariate analyses indicated that morphological variation is not distributed at random with respect to flowering times. Spatial autocorrelation analyses showed that temporal and spatial patterns were tightly linked. Interestingly, despite the fact that the population shows isolation by time, neighbourhood size and historical dispersal variance (σ̂ = 63 m) are similar to those detected in pure stands of F. excelsior where individuals flower rather synchronously and hermaphrodites are not the most frequent sexual type. Trees flowering at intermediate dates, which comprised the majority of the population, produced on average more flowers and fruits. We detected no significant differences in floral parasite infections relative to reproductive timing, although there was a tendency for late flowering trees to suffer from more gall attack. We discuss the impact of temporal variation in fitness traits and their possible role in the maintenance of the hybrid zone.

Sex Chromosome Drive

Sex chromosome drivers are selfish elements that subvert Mendels first law of segregation and therefore are overrepresented among the products of meiosis. The sex-biased progeny produced then fuels an extended genetic conflict between the driver and the rest of the genome. Many examples of sex chromosome drive are known, but the occurrence of this phenomenon is probably largely underestimated because of the difficulty to detect it. Remarkably, nearly all sex chromosome drivers are found in two clades, Rodentia and Diptera. Although very little is known about the molecular and cellular mechanisms of drive, epigenetic processes such as chromatin regulation could be involved in many instances. Yet, its evolutionary consequences are far-reaching, from the evolution of mating systems and sex determination to the emergence of new species.

Rapid evolution of a Y-chromosome heterochromatin protein underlies sex chromosome meiotic drive.

Significance Intragenomic conflict between the sex chromosomes is a strong evolutionary force. It can arise through the evolution of sex chromosome meiotic drive, where selfish genes located on the X chromosome promote their own transmission at the expense of the Y chromosome. Sex chromosome drive occurs in Drosophila simulans, where Paris drive results from segregation failure of the heterochromatic Y chromosome during meiosis II. Here, we show that Paris drive is caused by deficient alleles of the fast-evolving X-linked heterochromatin protein 1 D2 (HP1D2) gene. Our results suggest that dysfunctional HP1D2 alleles promote their own transmission, because they do not prepare the Y chromosome for meiosis. This finding shows that the rapid evolution of genes involved in heterochromatin structure can fuel intragenomic conflict. Sex chromosome meiotic drive, the non-Mendelian transmission of sex chromosomes, is the expression of an intragenomic conflict that can have extreme evolutionary consequences. However, the molecular bases of such conflicts remain poorly understood. Here, we show that a young and rapidly evolving X-linked heterochromatin protein 1 (HP1) gene, HP1D2, plays a key role in the classical Paris sex-ratio (SR) meiotic drive occurring in Drosophila simulans. Driver HP1D2 alleles prevent the segregation of the Y chromatids during meiosis II, causing female-biased sex ratio in progeny. HP1D2 accumulates on the heterochromatic Y chromosome in male germ cells, strongly suggesting that it controls the segregation of sister chromatids through heterochromatin modification. We show that Paris SR drive is a consequence of dysfunctional HP1D2 alleles that fail to prepare the Y chromosome for meiosis, thus providing evidence that the rapid evolution of genes controlling the heterochromatin structure can be a significant source of intragenomic conflicts.

Local dynamics of a fast-evolving sex-ratio system in Drosophila simulans

By distorting Mendelian transmission to their own advantage, X‐linked meiotic drive elements can rapidly spread in natural populations, generating a sex‐ratio bias. One expected consequence is the triggering of a co‐evolutionary arms race between the sex chromosome that carries the distorter and suppressors counteracting its effect. Such an arms race has been theoretically and experimentally established and can have many evolutionary consequences. However, its dynamics in contemporary populations is still poorly documented. Here, we investigate the fate of the young X‐linked Paris driver in Drosophila simulans from sub‐Saharan Africa to the Middle East. We provide the first example of the early dynamics of distorters and suppressors: we find consistent evidence that the driving chromosomes have been rising in the Middle East during the last decade. In addition, identical haplotypes are at high frequencies around the two co‐evolving drive loci in remote populations, implying that the driving X chromosomes share a recent common ancestor and suggesting that East Africa could be the cradle of the Paris driver. The segmental duplication associated with drive presents an unusual structure in West Africa, which could reflect a secondary state of the driver. Together with our previous demonstration of driver decline in the Indian Ocean where suppression is complete, these data provide a unique picture of the complex dynamics of a co‐evolutionary arms race currently taking place in natural populations of D. simulans.