Gametic specialization of centromeric histone paralogs in Drosophila virilis

In most eukaryotes, centromeric histone (CenH3) proteins mediate mitosis and meiosis and ensure epigenetic inheritance of centromere identity. We hypothesized that disparate chromatin environments in soma versus germline might impose divergent functional requirements on single CenH3 genes, which could be ameliorated by gene duplications and subsequent specialization. Here, we analyzed the cytological localization of two recently identified CenH3 paralogs, Cid1 and Cid5, in Drosophila virilis using specific antibodies and epitope-tagged transgenic strains. We find that only ancestral Cid1 is present in somatic cells, whereas both Cid1 and Cid5 are expressed in testes and ovaries. However, Cid1 is lost in male meiosis but retained throughout oogenesis, whereas Cid5 is lost during female meiosis but retained in mature sperm. Following fertilization, only Cid1 is detectable in the early embryo, suggesting that maternally deposited Cid1 is rapidly loaded onto paternal centromeres during the protamine-to-histone transition. Our studies reveal mutually exclusive gametic specialization of divergent CenH3 paralogs. Duplication and divergence might allow essential centromeric genes to resolve an intralocus conflict between maternal and paternal centromeric requirements in many animal species.

Dispersal alters the nature and scope of sexually antagonistic variation

Intra-locus sexual conflict, or sexual antagonism, occurs when alleles have opposing fitness effects in the two sexes. Previous theory suggests that sexual antagonism is a driver of genetic variation by generating balancing selection. However, these studies assume that populations are well-mixed, neglecting the effects of spatial subdivision. Here we use mathematical modelling to show that limited dispersal can fundamentally change evolution at sexually antagonistic autosomal and X-linked loci due to inbreeding and sex-specific kin competition. We find that if the sexes disperse at different rates, kin competition within the philopatric sex biases intralocus conflict in favour of the more dispersive sex. Furthermore, kin competition diminishes the strength of balancing selection relative to genetic drift, reducing genetic variation in small subdivided populations. Meanwhile, by decreasing heterozygosity, inbreeding reduces the scope for sexually antagonistic polymorphism due to non-additive allelic effects, and this occurs to a greater extent on the X-chromosome than autosomes. Overall, our results demonstrate that spatial structure is an important factor in predicting where to expect sexually antagonistic alleles. We suggest that observed interspecific and intragenomic variation in sexual antagonism may be explained by sex-specific dispersal ecology and demography.

Ancient Coretention of Paralogs of Cid Centromeric Histones and Cal1 Chaperones in Mosquito Species

Despite their essential role in chromosome segregation in most eukaryotes, centromeric histones (CenH3s) evolve rapidly and are subject to gene turnover. We previously identified four instances of gene duplication and specialization of Cid, which encodes for the CenH3 in Drosophila. We hypothesized that retention of specialized Cid paralogs could be selectively advantageous to resolve the intralocus conflict that occurs on essential genes like Cid, which are subject to divergent selective pressures to perform multiple functions. We proposed that intralocus conflict could be a widespread phenomenon that drives evolutionary innovation in centromeric proteins. If this were the case, we might expect to find other instances of coretention and specialization of centromeric proteins during animal evolution. Consistent with this hypothesis, we find that most mosquito species encode two CenH3 (mosqCid) genes, mosqCid1 and mosqCid2, which have been coretained for over 150 My. In addition, Aedes species encode a third mosqCid3 gene, which arose from an independent gene duplication of mosqCid1. Like Drosophila Cid paralogs, mosqCid paralogs evolve under different selective constraints and show tissue-specific expression patterns. Analysis of mosqCid N-terminal protein motifs further supports the model that mosqCid paralogs have functionally diverged. Extending our survey to other centromeric proteins, we find that all Anopheles mosquitoes encode two CAL1 paralogs, which are the chaperones that deposit CenH3 proteins at centromeres in Diptera, but a single CENP-C paralog. The ancient coretention of paralogs of centromeric proteins adds further support to the hypothesis that intralocus conflict can drive their coretention and functional specialization.

Gametic specialization of centromeric histone paralogs in Drosophila virilis

In most eukaryotes, centromeric histone (CenH3) proteins mediate the highly conserved process of chromosome segregation as the foundational kinetochore assembly factor. However, in multicellular organisms, CenH3 proteins have to perform their essential functions in different chromatin environments. CenH3 proteins not only mediate mitosis and meiosis but also ensure epigenetic inheritance of centromere identity on sperm chromatin, which is highly compact and almost completely stripped of histones during spermiogenesis. We hypothesized that such disparate chromatin environments might impose different functional constraints on CenH3. If so, gene duplications could ameliorate the difficulty of encoding divergent and even potentially incompatible centromeric functions in the same gene. Here, we analyzed the cytological localization of two recently identified CenH3 paralogs, Cid1 and Cid5, in D. virilis using specific antibodies and epitope-tagged transgenic strains. We find that only ancestral Cid1 is present in somatic cells, whereas both Cid1 and Cid5 are expressed in testes and ovaries. However, Cid1 and Cid5 are alternately retained in male and female gametes; Cid1 is lost in male meiosis but retained throughout oogenesis, whereas Cid5 is lost during female meiosis but retained in mature sperm. Following fertilization, maternally deposited Cid1 rapidly replaces paternal Cid5 during the protamine-to-histone transition. Our studies reveal mutually exclusive gametic specialization of two divergent CenH3 paralogs. We suggest that centromeric histone duplication and divergence may allow essential genes involved in chromosome segregation to specialize and thereby resolve an intralocus conflict between maternal and paternal centromeric histone requirements in many animal species.

Detecting sexual conflict and sexually antagonistic coevolution

We begin by providing an operational definition of sexual conflict that applies to both inter- and intralocus conflict. Using this definition, we examine a series of simple coevolutionary models to elucidate fruitful approaches for detecting interlocus sexual conflict and resultant sexually antagonistic coevolution. We then use published empirical examples to illustrate the utility of these approaches. Three relevant attributes emerge. First, the dynamics of sexually antagonistic coevolution may obscure the conflict itself. Second, competing models of inter-sexual coevolution may yield similar population patterns near equilibria. Third, a variety of evolutionary forces underlying competing models may be acting simultaneously near equilibria. One main conclusion is that studies of emergent patterns in extant populations (e.g. studies of population and/or female fitness) are unlikely to allow us to distinguish among competing coevolutionary models. Instead, we need more research aimed at identifying the forces of selection acting on shared traits and sexually antagonistic traits. More specifically, we need a greater number of functional studies of female traits as well as studies of the consequences of both male and female traits for female fitness. A mix of selection and manipulative studies on these is likely the most promising route.