Cospeciation vs host-shift speciation: methods for testing, evidence from natural associations and relation to coevolution.

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.

Sex in Penicillium: combined phylogenetic and experimental approaches.

We studied the mode of reproduction and its evolution in the fungal subgenus Penicillium Biverticillium using phylogenetic and experimental approaches. We sequenced mating type (MAT) genes and nuclear DNA fragments in sexual and putatively asexual species. Examination of the concordance between individual trees supported the recognition of the morphological species. MAT genes were detected in two putatively asexual species and were found to evolve mostly under purifying selection, although high substitution rates were detected at some sites in some clades. The first steps of sexual reproduction could be induced under controlled conditions in one of the two species, although no mature cleistothecia were produced. Altogether, these findings suggest that the asexual Penicillium species may have lost sex only very recently and/or that the MAT genes are involved in other functions. An ancestral state reconstruction analysis indicated several events of putative sex loss in the genus. Alternatively, it is possible that the supposedly asexual Penicillium species may have retained a cryptic sexual stage.

Phylogenetic determinants of potential host shifts in fungal pathogens.

Understanding what determines the host range of pathogens and the potential for host shifts is of critical importance to controlling their introductions into new environments. The phylogeny of the hosts has been shown to be important: pathogens are more likely to be infectious on hosts closely related to their host-of-origin because of the similar host environments that is shared by descent. The importance of pathogen phylogenies for predicting host range has never been investigated, although a pathogen should also be able to exploit a new host that its close relative can infect. We performed cross-inoculations using a plant-fungal association and showed that both host and pathogen phylogenies were significant predictors of host range, with at least partly independent effects. Furthermore, we showed that some pathogens were better at infecting novel hosts. Our results should have implications in the context of biological invasions and emergences of new diseases due to globalization.

Hybrid sterility and inviability in the parasitic fungal species complex Microbotryum.

Microbotryum violaceum, the anther-smut fungus, forms a complex of sibling species which specialize on different plants. Previous studies have shown the presence of partial ecological isolation and F1 inviability, but did not detect assortative mating apart from a high selfing rate. We investigated other post-mating barriers and show that F1 hybrid sterility, the inability of gametes to mate, increased gradually with the increasing genetic distance between the parents. F2 hybrids showed a reduced ability to infect the plants that was also correlated with the genetic distance. The host on which the F2 hybrids were passaged caused a selection for alleles derived from the pathogen species originally isolated from that host, but this effect was not detectable for the most closely related species. The post-mating barriers thus remain weak among the closest species pairs, suggesting that premating barriers are sufficient to initiate divergence in this system.

PERMANENT GENETIC RESOURCES: Isolation of 60 polymorphic microsatellite loci in EST libraries of four sibling species of the phytopathogenic fungal complex Microbotryum.

We report the development of 60 microsatellite markers on four species of the fungal complex Microbotryum, causing anther smut of the Caryophyllaceae. Microsatellites were found in four expressed sequence tag (EST) libraries, built from isolates of M. lychnis-dioicae, M. violaceum sensus stricto, M. lagerheimii and M. dianthorum, collected, respectively, from the plants Silene latifolia, S. nutans, S. vulgaris and Dianthus carthusianorum. Intrapopulation polymorphism was investigated using 24 isolates, and cross-amplification was explored using 23 isolates belonging to at least 10 different Microbotryum species. This study provides numerous microsatellite markers for population genetics and mapping studies.

When can host shifts produce congruent host and parasite phylogenies? A simulation approach.

Congruence between host and parasite phylogenies is often taken as evidence for cospeciation. However, 'pseudocospeciation', resulting from host-switches followed by parasite speciation, may also generate congruent trees. To investigate this process and the conditions favouring its appearance, we here simulated the adaptive radiation of a parasite onto a new range of hosts. A very high congruence between the host tree and the resulting parasite trees was obtained when parasites switched between closely related hosts. Setting a shorter time lag for speciation after switches between distantly related hosts further increased the degree of congruence. The shape of the host tree, however, had a strong impact, as no congruence could be obtained when starting with highly unbalanced host trees. The strong congruences obtained were erroneously interpreted as the result of cospeciations by commonly used phylogenetic software packages despite the fact that all speciations resulted from host-switches in our model. These results highlight the importance of estimating the age of nodes in host and parasite phylogenies when testing for cospeciation and also demonstrate that the results obtained with software packages simulating evolutionary events must be interpreted with caution.