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347I.348II.349III.349IV.355V.378VI.381381References381Glossary379 Summary: Hosts and their symbionts are involved in intimate physiological and ecological interactions. The impact of these interactions on the evolution of each partner depends on the time‐scale considered. Short‐term dynamics – ‘coevolution’ in the narrow sense – has been reviewed elsewhere. We focus here on the long‐term evolutionary dynamics of cospeciation and speciation following host shifts. Whether hosts and their symbionts speciate in parallel, by cospeciation, or through host shifts, is a key issue in host–symbiont evolution. In this review, we first outline approaches to compare divergence between pairwise associated groups of species, their advantages and pitfalls. We then consider recent insights into the long‐term evolution of host–parasite and host–mutualist associations by critically reviewing the literature. We show that convincing cases of cospeciation are rare (7%) and that cophylogenetic methods overestimate the occurrence of such events. Finally, we examine the relationships between short‐term coevolutionary dynamics and long‐term patterns of diversification in host–symbiont associations. We review theoretical and experimental studies showing that short‐term dynamics can foster parasite specialization, but that these events can occur following host shifts and do not necessarily involve cospeciation. Overall, there is now substantial evidence to suggest that coevolutionary dynamics of hosts and parasites do not favor long‐term cospeciation. [ABSTRACT FROM AUTHOR]

Divergent evolution of genomes among closely related species is shaped by both neutral processes and ecological forces, such as local adaptation and reinforcement. These factors can drive accelerated evolution of sex chromosomes relative to autosomes. Comparative genomic analyses between allopatric and sympatric species with overlapping or divergent ecological niches offer insights into reinforcement and ecological specialization on genome evolution. In the butterfly genus Morpho, several species coexist in sympatry, with specialization across forest strata and temporal niches. We analyzed the genomes of eight Morpho species, along with previously published genomes of three others, to compare chromosomal rearrangements and signs of positive selection in the Z chromosome vs autosomes. We found extensive chromosomal rearrangements in Z chromosome, particularly in sympatric species with similar ecological niches, suggesting a role for inversions in restricting gene flow at a postzygotic level. Z-linked genes also exhibited significantly higher dN/dS ratios than autosomal genes across the genus, with pronounced differences in closely related species living in sympatry. Additionally, we examined the evolution of eight circadian clock genes, detecting positive selection in Period, located on the Z chromosome. Our findings suggest that the Z chromosome evolves more rapidly than autosomes, particularly among closely related species, raising questions about its role in pre- and post-zygotic isolation mechanisms., (© The Author(s) 2024. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.)

The genomic processes enabling speciation and species coexistence in sympatry are still largely unknown. Here we describe the whole-genome sequencing and assembly of 3 closely related species from the butterfly genus Morpho: Morpho achilles (Linnaeus, 1758), Morpho helenor (Cramer, 1776), and Morpho deidamia (Höbner, 1819). These large blue butterflies are emblematic species of the Amazonian rainforest. They live in sympatry in a wide range of their geographical distribution and display parallel diversification of dorsal wing color pattern, suggesting local mimicry. By sequencing, assembling, and annotating their genomes, we aim at uncovering prezygotic barriers preventing gene flow between these sympatric species. We found a genome size of  480 Mb for the 3 species and a chromosomal number ranging from 2n = 54 for M. deidamia to 2n = 56 for M. achilles and M. helenor. We also detected inversions on the sex chromosome Z that were differentially fixed between species, suggesting that chromosomal rearrangements may contribute to their reproductive isolation. The annotation of their genomes allowed us to recover in each species at least 12,000 protein-coding genes and to discover duplications of genes potentially involved in prezygotic isolation like genes controlling color discrimination (L-opsin). Altogether, the assembly and the annotation of these 3 new reference genomes open new research avenues into the genomic architecture of speciation and reinforcement in sympatry, establishing Morpho butterflies as a new eco-evolutionary model., (© The Author(s) 2023. Published by Oxford University Press GigaScience.)

Background: Penicillium roqueforti is a filamentous fungus used for making blue cheeses worldwide. It also occurs as a food spoiler and in silage and wood. Previous studies have revealed a strong population genetic structure, with specific traits associated with the different populations. Here, we used a large strain collection from worldwide cheeses published recently to investigate the genetic structure of P. roqueforti., Principal Findings: We found a genetic population structure in P. roqueforti that was consistent with previous studies, with two main genetic clusters (W+C+ and W-C-, i.e., with and without horizontal gene transferred regions CheesyTer and Wallaby). In addition, we detected a finer genetic subdivision that corresponded to the environment and to protected designation of origin (PDO), namely the Roquefort PDO. We indeed found evidence for eight genetic clusters, one of the cluster including only strains from other environments than cheeses, and another cluster encompassing only strains from the Roquefort PDO. The W-C- and W+C+ cheese clusters were not the most closely related ones, suggesting that there may have been two independent domestication events of P. roqueforti for making blue cheeses., Significance: The additional population structure revealed here may be relevant for cheese-makers and for understanding the history of domestication in P. roqueforti.

Genetic differentiation occurs when gene flow is prevented, due to reproductive barriers or asexuality. Investigating the early barriers to gene flow is important for understanding the process of speciation. Here, we therefore investigated reproductive isolation between different genetic clusters of the fungus Penicillium roqueforti, used for maturing blue cheeses, and also occurring as food spoiler or in silage. We investigated premating and postmating fertility between and within three genetic clusters (two from cheese and one from other substrates), and we observed sexual structures under scanning electron microscopy. All intercluster types of crosses showed some fertility, suggesting that no intersterility has evolved between domesticated and wild populations despite adaptation to different environments and lack of gene flow. However, much lower fertility was found in crosses within the cheese clusters than within the noncheese cluster, suggesting reduced fertility of cheese strains, which may constitute a barrier to gene flow. Such degeneration may be due to bottlenecks during domestication and/or to the exclusive clonal replication of the strains in industry. This study shows that degeneration has occurred rapidly and independently in two lineages of a domesticated species. Altogether, these results inform on the processes and tempo of degeneration and speciation., (© 2016 The Author(s). Evolution © 2016 The Society for the Study of Evolution.)

Domestication is an excellent model for studies of adaptation because it involves recent and strong selection on a few, identified traits [1-5]. Few studies have focused on the domestication of fungi, with notable exceptions [6-11], despite their importance to bioindustry [12] and to a general understanding of adaptation in eukaryotes [5]. Penicillium fungi are ubiquitous molds among which two distantly related species have been independently selected for cheese making-P. roqueforti for blue cheeses like Roquefort and P. camemberti for soft cheeses like Camembert. The selected traits include morphology, aromatic profile, lipolytic and proteolytic activities, and ability to grow at low temperatures, in a matrix containing bacterial and fungal competitors [13-15]. By comparing the genomes of ten Penicillium species, we show that adaptation to cheese was associated with multiple recent horizontal transfers of large genomic regions carrying crucial metabolic genes. We identified seven horizontally transferred regions (HTRs) spanning more than 10 kb each, flanked by specific transposable elements, and displaying nearly 100% identity between distant Penicillium species. Two HTRs carried genes with functions involved in the utilization of cheese nutrients or competition and were found nearly identical in multiple strains and species of cheese-associated Penicillium fungi, indicating recent selective sweeps; they were experimentally associated with faster growth and greater competitiveness on cheese and contained genes highly expressed in the early stage of cheese maturation. These findings have industrial and food safety implications and improve our understanding of the processes of adaptation to rapid environmental changes., (Copyright © 2015 The Authors. Published by Elsevier Ltd.. All rights reserved.)

Fungi exhibit substantial morphological and genetic diversity, often associated with cryptic species differing in ecological niches. Penicillium roqueforti is used as a starter culture for blue-veined cheeses, being responsible for their flavor and color, but is also a common spoilage organism in various foods. Different types of blue-veined cheeses are manufactured and consumed worldwide, displaying specific organoleptic properties. These features may be due to the different manufacturing methods and/or to the specific P. roqueforti strains used. Substantial morphological diversity exists within P. roqueforti and, although not taxonomically valid, several technological names have been used for strains on different cheeses (e.g., P. gorgonzolae, P. stilton). A worldwide P. roqueforti collection from 120 individual blue-veined cheeses and 21 other substrates was analyzed here to determine (i) whether P. roqueforti is a complex of cryptic species, by applying the Genealogical Concordance Phylogenetic Species Recognition criterion (GC-PSR), (ii) whether the population structure assessed using microsatellite markers correspond to blue cheese types, and (iii) whether the genetic clusters display different morphologies. GC-PSR multi-locus sequence analyses showed no evidence of cryptic species. The population structure analysis using microsatellites revealed the existence of highly differentiated populations, corresponding to blue cheese types and with contrasted morphologies. This suggests that the population structure has been shaped by different cheese-making processes or that different populations were recruited for different cheese types. Cheese-making fungi thus constitute good models for studying fungal diversification under recent selection.

The level of parasite virulence, i.e., the decrease in host's fitness due to a pathogen, is expected to depend on several parameters, such as the type of the disease (e.g., castrating or host-killing) and the prevalence of multiple infections. Although these parameters have been extensively studied theoretically, few empirical data are available to validate theoretical predictions. Using the anther smut castrating disease on Silene latifolia caused by Microbotryum lychnidis-dioicae, we studied the dynamics of multiple infections and of different components of virulence (host death, non-recovery and percentage of castrated stems) during the entire lifespan of the host in an experimental population. We monitored the number of fungal genotypes within plants and their relatedness across five years, using microsatellite markers, as well as the rates of recovery and host death in the population. The mean relatedness among genotypes within plants remained at a high level throughout the entire host lifespan despite the dynamics of the disease, with recurrent new infections. Recovery was lower for plants with multiple infections compared to plants infected by a single genotype. As expected for castrating parasites, M. lychnidis-dioicae did not increase host mortality. Mortality varied across years but was generally lower for plants that had been diseased the preceding year. This is one of the few studies to have empirically verified theoretical expectations for castrating parasites, and to show particularly i) that castrated hosts live longer, suggesting that parasites can redirect resources normally used in reproduction to increase host lifespan, lengthening their transmission phase, and ii) that multiple infections increase virulence, here in terms of non-recovery and host castration.

The emblematic fungus Penicillium roqueforti is used throughout the world as a starter culture in the production of blue-veined cheeses. Like other industrial filamentous fungi, P. roqueforti was thought to lack a sexual cycle. However, an ability to induce recombination is of great economic and fundamental importance, as it would make it possible to transform and improve industrial strains, promoting the creation of novel phenotypes and eliminating the deleterious mutations that accumulate during clonal propagation. We report here, for the first time, the induction of the sexual structures of P. roqueforti - ascogonia, cleistothecia and ascospores. The progeny of the sexual cycle displayed clear evidence of recombination. We also used the recently published genome sequence for this species to develop microsatellite markers for investigating the footprints of recombination and population structure in a large collection of isolates from around the world and from different environments. Indeed, P. roqueforti also occurs in silage, wood and human-related environments other than cheese. We found tremendous genetic diversity within P. roqueforti, even within cheese strains and identified six highly differentiated clusters that probably predate the use of this species for cheese production. Screening for phenotypic and metabolic differences between these populations could guide future development strategies.

Although most eukaryotes reproduce sexually at some moment of their life cycle, as much as a fifth of fungal species were thought to reproduce exclusively asexually. Nevertheless, recent studies have revealed the occurrence of sex in some of these supposedly asexual species. For industrially relevant fungi, for which inoculums are produced by clonal-subcultures since decades, the potentiality for sex is of great interest for strain improvement strategies. Here, we investigated the sexual capability of the fungus Penicillium roqueforti, used as starter for blue cheese production. We present indirect evidence suggesting that recombination could be occurring in this species. The screening of a large sample of strains isolated from diverse substrates throughout the world revealed the existence of individuals of both mating types, even in the very same cheese. The MAT genes, involved in fungal sexual compatibility, appeared to evolve under purifying selection, suggesting that they are still functional. The examination of the recently sequenced genome of the FM 164 cheese strain enabled the identification of the most important genes known to be involved in meiosis, which were found to be highly conserved. Linkage disequilibria were not significant among three of the six marker pairs and 11 out of the 16 possible allelic combinations were found in the dataset. Finally, the detection of signatures of repeat induced point mutations (RIP) in repeated sequences and transposable elements reinforces the conclusion that P. roqueforti underwent more or less recent sex events. In this species of high industrial importance, the induction of a sexual cycle would open the possibility of generating new genotypes that would be extremely useful to diversify cheese products.

Critical determinants of the optimum level of virulence in pathogens include the presence of competitors (i.e., multiple infections), their relatedness, and the effect of competitors on pathogen growth and disease development. Empirical data regarding the existence of competitive interactions and their impact on virulence remain very limited compared to theoretical studies. Here, we followed an experimental population of the model fungal pathogen Microbotryum lychnidis-dioicae on its caryophyllaceous host Silene latifolia. Our analysis revealed conditional responses by the pathogen to the presence of competitors, which was dependent upon the relatedness of pathogens within hosts. Overall, virulence was increased in cases of multiple infections as compared to single infections: both spore production and degree of plant sterilization were higher under multiple infections. The pathogen indeed increased its growth and reproductive rate when competitors were present within the same plant. Microbotryum also appeared able to interfere with competitors, reducing their ability to colonize the host, and this effect was smaller between closer relatives. Our results thus help to elucidate the myriad of theoretical considerations on the evolution of virulence by providing experimental results with a well-studied disease of wild plant populations., (© 2010 The Author(s). Evolution© 2010 The Society for the Study of Evolution.)

Population models of host-parasite interactions predict that when different parasite genotypes compete within a host for limited resources, those that exploit the host faster will be selected, leading to an increase in parasite virulence. When parasites sharing a host are related, however, kin selection should lead to more cooperative host exploitation that may involve slower rates of parasite reproduction. Despite their potential importance, studies that assess the prevalence of multiple genotype infections in natural populations remain rare, and studies quantifying the relatedness of parasites occurring together as natural multiple infections are particularly scarce. We investigated multiple infections in natural populations of the systemic fungal plant parasite Microbotryum violaceum, the anther smut of Caryophyllaceae, on its host, Silene latifolia. We found that multiple infections can be extremely frequent, with different fungal genotypes found in different stems of single plants. Multiple infections involved parasite genotypes more closely related than would be expected based upon their genetic diversity or due to spatial substructuring within the parasite populations. Together with previous sequential inoculation experiments, our results suggest that M. violaceum actively excludes divergent competitors while tolerating closely related genotypes. Such an exclusion mechanism might explain why multiple infections were less frequent in populations with the highest genetic diversity, which is at odds with intuitive expectations. Thus, these results demonstrate that genetic diversity can influence the prevalence of multiple infections in nature, which will have important consequences for their optimal levels of virulence. Measuring the occurrence of multiple infections and the relatedness among parasites within hosts in natural populations may be important for understanding the evolutionary dynamics of disease, the consequences of vaccine use, and forces driving the population genetic structure of parasites.

In gynodioecious plant species, females are expected to have more resources available for maturing seeds because pistillate flowers are smaller, do not produce pollen, and are thus less costly that perfect flowers. The potential female advantage arising from more abundant resources is, however, likely to vary depending on whether seed production is limited by resource or pollen availability. Here we experimentally investigated the influence of pollen and resource limitation on female advantage in a gynodioecious species using two levels of pollination. Total seed production of females was always greater than that of hermaphrodites: females produced more flowers and more fruits that contained similar numbers of seeds of similar mass. Under low pollination, female and hermaphrodite plants allocated resources to increased flower production rather than to increased seed size or quality. We did not detect any influence of pollen or resource limitation on female advantage, which remained similar under low (= abundant resources) and full pollination. Outcrossed fruits performed better than selfed fruits when the same plant received both selfed and outcrossed pollen on different flowers. These differences were not greater under high pollination, possibly because resources available for each fruit did not differ between our pollen intensity treatments.

Females of gynodioecious species need to have reproductive advantages to compensate for their lack of male function and assure their maintenance in natural populations. Females may be more fecund than hermaphrodites because they reallocate resources from male to female function, avoid selfing and inbreeding depression, or produce higher quality offspring by screening arriving pollen better. A novel type of female advantage is proposed that may be important for several species of gynodioecious Caryophyllaceae. The anther smut fungus Microbotryum violaceum generally sterilizes its infected hosts but even without infection, spore deposition can negatively affect the reproduction of healthy individuals. In Gypsophila repens, flowers of hermaphrodite plants experimentally pollinated with both fungal spores and pollen produced significantly fewer fruits and seeds than those that received pollen alone, whereas female reproduction was unaffected by spore deposition. This unexplored reproductive advantage of females is probably due to the larger stigmatic surface in pistillate flowers, that allows pollen germination despite the presence of spores. Because longer stigmas may also lead to increased spore deposition, these results raise questions regarding the infection probability for each sex, possible sex-specific defense mechanisms, and the general role of pathogens in the maintenance of females in natural gynodioecious populations.

Female fecundity advantage in gynodioecious plants is required for the spread and maintenance of this reproductive system. However, not all reproductive characters show female advantage in all species. We used a meta-analysis to summarise differences between females and hermaphrodites reported from the literature for several reproductive traits. Further we tested three hypotheses, (1) that female plants of species with many ovules produce more seeds per fruit while those with few ovules produce heavier seeds, (2) that females are more pollen limited than hermaphrodites, and (3) that floral sexual size dimorphism is more pronounced in species with few ovules, either because female reproductive success is less limited by pollen availability in such species or because flowers with few ovules require a smaller floral structure to protect the carpels. Overall, females compared to hermaphrodites produced more but smaller flowers, had higher fruit set, higher total seed production, and produced heavier seeds that germinated better. Species with many versus few ovules differed in female advantage for flower size dimorphism, flower number, fruit set and total seed production. However seed size, seed set per fruit and seed germination differences between females and hermaphrodites did not differ significantly between species with few and many ovules. We also found no evidence for differential pollen limitation between females and hermaphrodites. Degree of floral sexual size dimorphism differed significantly between species with few and many ovules. Though pistillate flowers were generally smaller than those of hermaphrodites, species with many ovules showed less difference in flower size between the sexes, suggesting either that the protective role of the perianth constrains the evolution of sexual size dimorphism in species with many ovules or that selection for adequate pollination in species with many ovules impedes the reduction in flower size of females.