As you weed, so shall you reap: on the origin of algaculture in damselfish

Within their territories, damselfish cultivate particular algae for consumption. A recent study in BMC Evolutionary Biology shows extensive variation among and within fish species in the composition of these algal 'gardens', varying from monocultures to cultures of mixed species, and in the mode of cultivation. This fish-algal agriculture may provide insight into the early stages of domesticatio

Species and speciation in the Hebeloma crustuliniforme complex.

This thesis deals with species delimitation and speciation in the ectomycorrhizal Hebeloma crustuliniforme complex. The species concept traditionally used in this complex is based on morphology of basidiocarps. However, species delimitation has been controversial. One of the best known names is H. crustuliniforme (Bull.) Quél., a name regularly encountered in the mycorrhizal literature. However, this name has been used for a species complex of taxa with relatively pale (but sometimes more brown-tinged), veilless carpophores with weeping lamellae. In this thesis the basal criterion to delimit species within the Hebeloma crustuliniforme complex is sexual intercompatibility. Therefore, speciation is here defined as the origin of sexual interincompatibility. The strategy that has been used in this thesis to address the questions of species delimitation and speciation in the Hebeloma crustuliniforme complex can be summarized as follows:Define InterCompatibility Groups (ICGs) and look for examples of partial incompatibility (Chapter 2);Determine phylogenetic relationships between those ICGs (Chapter 3);Focus on closely related, and preferentially partially incompatible, ICGs to study speciation (Chapters 4, 5);Derive an operational species concept for the Hebeloma crustuliniforme complex that is based on morphological recognition of (combinations of) biological species within an explicitly phylogenetic framework (Chapter 6).In Chapter 2 the results are described of intercompatibility tests in this species complex. In a sample of 110 collections 20 InterCompatibility Groups (ICGs) were found. Partial compatibility was found between ICGs 3 and 4, between 2 and 3/4, between 1 and 2 and between 16 and 17. One strain (605) was compatible with all strains of ICGs 3 and 4. In all other cases, however, assignment of isolates to a single ICG was unambiguous. Individual compatible combinations between members of the partially compatible ICG 1 and 2 and between members of the partially compatible ICG 16 and 17 showed signs of reduced compatibility. This was reflected by: (i) no or unidirectional nuclear migration, (ii) reduced growth rate of the dikaryon and (iii) aberrant morphology of hyphae.In Chapter 3 phylogenetic relationships were studied between the ICGs of the H. crustuliniforme complex and between them and the other main groups in the genus Hebeloma based on nuclear ribosomal ITS sequences, using cladistic methods. The 20 ICGs of the H. crustuliniforme complex do not form a monophyletic group, but instead form two distinct clades, one consisting of three ICGs (clade I) and the other of 17 ICGs (clade II). Most of the ICGs in the latter clade were very closely related as suggested by a low sequence divergence. The majority of ICGs of this clade showed a preference for Salicaceae , but the basal ICG (ICG 21) did not. The host tree switch to Salicaceae has probably been followed by extensive and rapid speciation.Several other well supported clades were found in the genus Hebeloma , but the basal relationships between them were not well resolved. It is therefore impossible to propose a new infrageneric division for Hebelama .In Chapter 4 a subclade of clade II (subclade IIa) was studied in detail. In this subclade nine ICGs were found, four of which were partially compatible. This partial intercompatibility was organised hierarchically with an intermediate level of compatibility between ICGs 3 and 4 and very limited compatibility between 2 and 3/4 and between 1 and 2. The single strain (605) that was intercompatible with all strains of ICGs 3 and 4 was a member of subclade IIa as well. A mitochondrial and a nuclear phylogeny of strains belonging to these partially compatible populations were reconstructed. For ICGs 2, 3 and 4 a positive correlation was found between the level of interincompatibility and the relative age of the most recent common ancestor. ICGs generally formed monophyletic groups, ICG 3 and 4 (15% partial intercompatibility) together formed a monophyletic group and the sister group of (3,4) was ICG 2 (0.4% intercompatible with (3,4)). This is consistent with a gradual origin of sexual incompatibility (divergence-first). ICG 1 had a different position in the nuclear and mitochondrial phylogeny. In the nuclear phylogeny it was the sister taxon of ICG 5, and in the mitochondrial the sister group of ICG 2. A possible explanation is that ICG 1 has a hybrid origin, with the ancestor of ICG 5 as the nuclear donor and the ancestor of 2 as the mitochondrial donor.The subject of Chapter 5 is a polymorphism in the ribosomal Internal Transcribed Spacer of ICG 17. Within this ICG of the morphospecies Hebeloma velutipes a dikaryotic strain (d504) was found with two divergent types ITS. These two types segregated in monokaryotic progeny of the same strain, showing that the different ITS types represent different alleles at homologous rDNA loci. RFLP analysis of more strains of ICG 17 showed that the polymorphism is widespread, with both types occurring in Europe as well as in America. Cladistic analyses of the two ITS sequences showed that they did not form a monophyletic group. One of the types belonged to a clade together with the single ITS type found in the partially compatible ICG 16 and the other to a clade together with the single ITS type found in the fully incompatible ICG 18. RFLP analysis of the mitochondrial ribosomal SSU showed that there were fixed differences between the mitochondria of ICG 16 and 17. Several lines of evidence were described that the ITS polymorphism in ICG 17 is not the result of actual hybridisation between 16 and 17. The polymorphism within ICG 17 must therefore be of a different origin. The lack of recombinants, neither within the rDNA locus nor between ITS 1 and 2, suggests that the two types have come together relatively recently. The ITS polymorphism described in this Chapter clearly showed the potential danger of using single ribosomal sequences for reconstructing species phylogenies and the potential problems for molecular identification of species.In Chapter 6 a method is presented to derive an operational species concept for the Hebeloma crustuliniforme complex that is based on (combinations of) biological species within an explicitly phylogenetic framework. Crucial in this analysis is a reliable estimate of the phylogeny of biological species in the H. crustuliniforme complex. Based on two nuclear sequences, we presented a best estimate of the phylogeny of biological species within the H. crustuliniforme complex. Using this phylogeny, on the basis of (strict) monophyly only two species could be recognised among 20 biological species, viz. H. velutipes and H. helodes . An earlier phylogenetic analysis indicated that these two morphological species are not sister taxa. Relaxing the criterion of monophyly and allowing paraphyletic groupings of biological species as a morphospecies resulted in the recognition of three morphospecies, viz. H. velutipes , H. incarnatulum and H. helodes . A tree, with the five ICGs of the previously defined morphospecies Hebeloma crustuliniforme (1, 2, 3, 4 and 5) constrained as a monophyletic group could not be rejected. This constrained tree, together with the relaxed criterion, allowed the recognition of four species, viz. H. helodes , H. crustuliniforme , H. velutipes and H. incarnatulum . The limited ability to translate a biological species concept into an operational species concept was explained by the lack of qualitative characters and the plasticity of quantitative characters. Based on the close relationship between the ICGs in the two clades of the H. crustuliniforme complex, it was shown that a good correspondence between a biological species concept and a morphological species concept is not likely to be forthcoming.In the final Chapter the results found in this study were integrated and discussed in a broader context and directions for future research were suggested. Future phylogenetic studies should consider the possibility of genetic exchange between divergent populations more explicitly.</p

A widely distributed ITS polymorphism within a biological species of the ectomycorrhizal fungus Hebeloma velutipes

The ectomycorrhizal fungus Hebeloma velutipes consists of two biological species (BSP 16 and 17). Within BSP 17 a dikaryon was found with two divergent types of the ribosomal Internal Transcribed Spacer (ITS1 and 2). The two ITS types segregated in monokaryotic progeny of that dikaryon, showing that these different ITS types represent different alleles at homologous rDNA loci in the two nuclei. RFLP analysis of a number of strains of BSP 17 showed that the polymorphism is widespread in Europe. There was no deficiency of the heterokaryotic type, demonstrating that ITS divergence in this species is not correlated with reduced intercompatibility. A strain from North America, not assigned to a biological species, showed the same polymorphism. Cladistic analysis of the two ITS sequences showed that they were not sister groups. One of the ITS types formed a monophyletic group together with the ITS type of BSP 16, the other type formed a clade with the ITS type of H. incarnatulum (BSP 18). BSP 16 and 17 showed partial intercompatibility. However, several lines of evidence suggest that the polymorphism of BSP 17 is not the result of frequent and continuing hybridisation with BSP 16. Instead, we give arguments for the hypothesis that the polymorphism evolved in allopatry and that the two types have come together relatively recently. The results of the polymorphism indicate a potential problem for molecular identification of fungal species based on ITS fingerprinting. The results also show that no generalisations are possible about the relation of speciation (the formation of BSP) and nuclear ITS divergence

How a long-lived fungus keeps mutations in check

An individual of the mushroom-forming fungus Armillaria bulbosa is among the largest and oldest of all living organisms: More than 1500 years old, it covers more than 15 ha and weighs more than 10,000 kg (1). Some trees can also reach ages of thousands of years (2). How can such long-lived organisms keep the number of deleterious mutations during somatic growth in check? In a recent paper in Mycologia, Anderson and Catona (3) report extremely low genetic variation, and by inference a very low mutation rate, in a long-lived individual of another fungus, Armillaria gallica (see the photo). This genomic stability is puzzling and unexpected, because the sequenced samples come from locations that are more than 100 m apart and presumably separated by many rounds of cell divisio

Using the 'Buller phenomenon' in experimental evolution studies of basidiomycetes

In basidiomycetes, the monokaryons in a mating simultaneously exhibit two clearly distinct behaviors that can be considered as female and male roles, respectively: the acceptance of a nucleus, and the donation of a nucleus. However, since each monokaryon is a hermaphrodite, these two behaviors are difficult to distinguish. Here, I describe a simple method to select for the male role. A nucleus is serially passed through a non-evolving monokaryon, utilizing the ‘Buller phenomenon’. I describe some theoretical predictions that can be tested with this method. Sexual reproduction in basidiomycetes starts with hyphal fusion between two monokaryons (haploid mycelia arising after spore germination; c.f. Casselton and Economou, 1985; Raper 1966). Subsequently, haploid nuclei are exchanged and reciprocally migrate throughout the existing mycelia to give rise to a dikaryon (Figure 1a). Figure 1. A. The standard life cycle of a heterothallic basidiomycete fungus. Sexual spores germinate (upper left) give rise to a haploid monokaryon. Two compatible monokaryons can fuse, upon which they reciprocally exchange nuclei, without cytoplasmic mixing (down left). This leads to the formation of the dikaryon (grey, right), all cells of which have two different nuclei, and which is a cytoplasmic mosaic. The dikaryon can produce mushrooms (schematically drawn on the grey dikaryon), the sexual fruiting bodies, where a short diploid stage is immediately followed by meiosis and sexual spore formation. The insert shows how the two nuclei in a dikaryotic cell are distributed over cells during cell division via the formation of clamp connections. B. The monokaryons exhibit two clearly distinct behaviors in a mating, accepting a nucleus, and donating

The costs of being male: are there sex-specific effects of uniparental mitochondrial inheritance?

Eukaryotic cells typically contain numerous mitochondria, each with multiple copies of their own genome, the mtDNA. Uniparental transmission of mitochondria, usually via the mother, prevents the mixing of mtDNA from different individuals. While on the one hand, this should resolve the potential for selection for fast-replicating mtDNA variants that reduce organismal fitness, maternal inheritance will, in theory, come with another set of problems that are specifically relevant to males. Maternal inheritance implies that the mitochondrial genome is never transmitted through males, and thus selection can target only the mtDNA sequence when carried by females. A consequence is that mtDNA mutations that confer male-biased phenotypic expression will be prone to evade selection, and accumulate. Here, we review the evidence from the ecological, evolutionary and medical literature for male specificity of mtDNA mutations affecting fertility, health and ageing. While such effects have been discovered experimentally in the laboratory, their relevance to natural populations—including the human population—remains unclear. We suggest that the existence of male expression-biased mtDNA mutations is likely to be a broad phenomenon, but that these mutations remain cryptic owing to the presence of counter-adapted nuclear compensatory modifier mutations, which offset their deleterious effect

The evolution of obligate mutualism: if you can't beat

Wolbachia is best known as a facultative endosymbiotic parasite, manipulating host reproduction. However, it has also evolved as an obligate mutualist at least twice. In a recent paper, Pannebakker et al. identify a possible mechanism for such a transition from facultative parasitism to obligate mutualism in a parasitic wasp in which Wolbachia are required for producing eggs (oogenesis). Their proposed mechanism suggests that compensatory evolution in the host to counter the harmful effects of Wolbachia is the basis of this evolutionary transition

Asymmetrical template-DNA strand segregation can explain density-associated mutation-rate plasticity

The mutation rate is a fundamental factor in evolutionary genetics. Recently, mutation rates were found to be strongly reduced at high density in a wide range of unicellular organisms, prokaryotic and eukaryotic. Independently, cell division was found to become more asymmetrical at increasing density in diverse organisms; in yeast, some "mother" cells continue dividing, while their "offspring" cells do not divide further. Here, we investigate how this increased asymmetry in cell division at high density can be reconciled with reduced mutation-rate estimates. We calculated the expected number of mutant cells due to replication errors under various modes of segregation of template-DNA strands and copy-DNA strands, both under exponential and under linear growth. We show that the observed reduction in the mutation rate at high density can be explained if mother cells preferentially retain the template-DNA strands, since new mutations are then confined to non-dividing daughter cells thus reducing the spread of mutant cells. Any other inheritance mode results in an increase in the number of mutant cells at higher density. The proposed hypothesis that patterns of DNA-strand segregation are density dependent fundamentally challenges our current understanding of mutation-rate estimates and extends the distinction between germline and soma to unicellular organisms

The birth of cooperation

Mutually beneficial associations between individuals of different species, called mutualistic symbioses, have enabled major ecological innovations and underlie some of the major transitions in evolution (1). For example, the ancestor of plants domesticated endosymbiotic photosynthetic bacteria, today's chloroplasts, for carbon fixation. This association dramatically increased the habitat of these photosynthetic bacteria from the sea to terrestrial ecosystems. However, the colonization of land by plants required an additional symbiotic association, with fungal root symbionts that facilitate nutrient uptake (2). Yet, surprisingly little is known about how mutualistic symbioses evolved and persist. On page 94 of this issue, Hom and Murray show how mutualism may arise without prior coevolution (see the photo) (3