Jean-Yves Rasplus

Mutualists with attitude: coevolving fig wasps and figs

The intimate mutualism between fig wasps and figs has long captivated biologists, and new phylogenies are now uncovering its evolutionary history. Fig-pollinating wasps evolved just once, but fig parasitism has evolved repeatedly and convergently. Figs and their pollinators appear to have co-speciated considerably, but not invariably, because the famous one-to-one rule of specificity is often broken. Some key traits of figs and pollinators show impressive correlated evolution, but the resolution of conflicts that threaten the stability of the mutualism remains controversial.

High similarity between flanking regions of different microsatellites detected within each of two species of Lepidoptera: Parnassius apollo and Euphydryas aurinia.

Microsatellite flanking regions have been compared in two butterfly species. Several microsatellite flanking regions showed high similarity to one another among different microsatellites within a same species, but very few similarities were found between species. This can be the consequence of either duplication/multiplication events involving large regions containing microsatellites or of microsatellites imbedded in minisatellite regions. The multiplication of microsatellites might also be linked to mobile elements. Furthermore, crossing over between nonhomologous microsatellites can lead to the exchange of the flanking regions between microsatellites. The same phenomenon was observed in both studied butterfly species but not in Aphis fabae (Hemiptera), which was screened at the same time using the same protocol. These findings might explain, at least partially, why microsatellite isolation in Lepidoptera has been relatively unsuccessful so far.

Alien Terrestrial Invertebrates of Europe

Unlike other groups of animals and plants, no checklist of alien terrestrial invertebrates was available in any of the European countries until recently. Since 2002, such checklists were successively provided by Austria (Essl and Rabitsch 2002), Germany (Geiter et al. 2002), the Czech Republic (Sefrova and Lastu vka 2005), Scandinavia (NOBANIS 2007), the United Kingdom (Hill et al. 2005), Switzerland (Wittenberg 2006) and Israel (Roll et al. 2007). However, most European regions remained uncovered and, furthermore, comparisons between the existing lists were inherently difficult because they used different definitions of alien. Thus, estimating the importance of terrestrial alien invertebrates at the European level remained impossible, mostly because of poor taxonomic knowledge existed for several groups. By gathering taxonomists and ecologists specialised on most invertebrate taxa together with collaborators working at the national level in 35 European countries, the DAISIE project intended to fill this gap. However, a lack of European expertise in some taxonomic groups did not allow coverage of all the terrestrial invertebrates with the same level of precision. Data on insects were more reliable than those of other taxa, and consequently the analyses presented below will mostly refer to this group.

Isolation by distance and sharp discontinuities in gene frequencies: implications for the phylogeography of an alpine insect species, Carabus solieri

Analysis of genetic isolation by distance (IBD) is of prime importance for the study of processes responsible for spatial population genetic structure and is thus frequently used in case studies. However, the identification of a significant IBD pattern does not necessarily imply the absence of sharp discontinuities in gene frequencies. Therefore, identifying barriers to gene flow and/or secondary contact between differentiated entities remains a major challenge in population biology. Geographical genetic structure of 41 populations (1080 individuals) of an alpine insect species, Carabus solieri, was studied using 10 microsatellite loci. All populations were significantly differentiated and spatially structured according to IBD over the entire range. However, clustering analyses clearly identified three main clusters of populations, which correspond to geographical entities. Whereas IBD also occurs within each cluster, population structure was different according to which group of populations was considered. The southernmost cluster corresponds to the most fragmented part of the range. Consistently, it was characterized by relatively high levels of differentiation associated with low genetic diversity, and the slope of the regression of genetic differentiation against geographical distances was threefold those of the two other clusters. Comparisons of within‐cluster and between‐cluster IBD patterns revealed barriers to gene flow. A comparison of the two approaches, IBD and clustering analyses, provided us with valuable information with which to infer the phylogeography of the species, and in particular to propose postglacial colonization routes from two potential refugia located in Italy and in southeastern France. Our study highlights strongly the possible confounding contribution of barriers to gene flow to IBD pattern and emphasizes the utility of the model‐based clustering analysis to identify such barriers.

CONVERGENCE AND COEVOLUTION IN A MUTUALISM: EVIDENCE FROM A MOLECULAR PHYLOGENY OF FICUS

Abstract The interaction between Ficus (Moraceae) and their pollinating wasps (Chalcidoidea: Agaonidae; more than 700 species-specific couples) is one of the most specialized mutualisms found in nature. Both partners of this interaction show extensive variation in their respective biology. Here we investigate Ficus life-history trait evolution and fig/fig wasp coadaptation in the context of a well-resolved molecular phylogeny. Mapping out variations in Ficus life-history traits on an independently derived phylogeny constructed from ribosomal DNA sequences (external and internal transcribed spacer) reveals several parallel transitions in Ficus growth habit and breeding system. Convergent trait evolution might explain the discrepancies between morphological analyses and our molecular reconstruction of the genus. Morphological characters probably correlate with growth habit and breeding system and could therefore be subject to convergent evolution. Furthermore, we reconstruct the evolution of Ficus inflorescence characters that are considered adaptations to the pollinators. Our phylogeny reveals convergences in ostiole shape, stigma morphology, and stamen:ovule ratio. Statistical tests taking into account the phylogenetic relationship of the species show that transitions in ostiole shape are correlated with variation in wasp pollinator head shape, and evolutionary changes in stigma morphology and stamen:ovule ratio correlate with changes in the pollination behavior of the associated wasp. These correlations provide evidence for reciprocal adaptations of morphological characters between these mutualistic partners that have interacted over a long evolutionary time. In light of previous ecological studies on mutualism, we discuss the adaptive significance of these correlations and what they can tell us about the coevolutionary process occurring between figs and their pollinators.

Non-Pollinating Afrotropical Fig Wasps Affect the Fig-Pollinator Mutualism in Ficus within the Subgenus Sycomorus

Ficus are species-specifically pollinated by chalcidoid wasps (Agaonidae), and the fig tree-fig pollinator mutualism has long been studied. A diversity of other chalcids, both gall-makers or parasitoids, co-occur in each monoecious Ficus species, and use the fig resource by developing in ovaries that they transform into galls. The oviposition sequence and impact on the mutualism of these non-pollinating fig wasps were studied on two Ficus species of the subgenus Sycomorus in the Ivory Coast. Field observations, fig measurements and counts of wasps and seeds from mature figs were conducted. Four groups of fig wasp species oviposit in the ovaries at different stages of syconial development, and were demonstrated to lay eggs in the internal ovary layers; the most external flowers seem to be protected against oviposition and thus develop into seeds. Non-pollinating wasp species, by parasitizing pollinator larvae or by competing for oviposition sites, have a significant negative impact on the pollinator population and dynamics, and thereby on Ficus male function (i.e. pollen dispersal). In contrast, but for one species, they do not affect the seed production, that is, the tree female function.

Fine-scale genetic structure of two carabid species with contrasted levels of habitat specialization

Using microsatellite markers, we compared the genetic structure of populations of two carabid species, one described as a generalist (commonly found in forest and in open habitats) and the other known as a forest specialist. Both species were sampled in the same forest plots, which were separated from each other by either open or forested areas. At the local scale considered (13.6 km separating the most distant plots), genetic differentiation was substantial for both species studied, but populations of the forest specialist Carabus punctatoauratus appeared to be more spatially structured than those of C. nemoralis. Isolation by distance analyses showed that nonforested areas are partial barriers to gene flow for both species studied, although more clearly for the forest specialist. Between and within forests, dispersal capacity of the generalist C. nemoralis was shown to be higher than that of the specialist C. punctatoauratus.

Pollination mode in fig wasps: the predictive power of correlated traits

The over 700 species of Ficus are thought to have co–speciated with their obligate pollinators (family Agaonidae). Some of these wasp species pollinate figs actively, while others are passive pollinators. Based on direct observations of mode of pollination in 88 species, we show that mode of pollination can confidently be predicted from fig traits only (anther–to–ovule ratio) or from wasp traits only (presence of coxal combs). The presence of pollen pockets is not a predictor of mode of pollination. Data, direct and indirect, on 142 species, demonstrate numerous cases of the loss of active pollination and suggest one or few origins of active pollination. Hence, active pollination, an impressive example of the sophisticated traits that may result from mutualistic coevolution, depends on selective forces that can be overcome in some species, allowing reversions. Despite frequent loss, active pollination remains the predominant mode of pollination in Ficus.

Population genetic structure of male black grouse (Tetrao tetrix L.) in fragmented vs. continuous landscapes

We investigated the association of habitat fragmentation with genetic structure of male black grouse Tetrao tetrix. Using 14 microsatellites, we compared the genetic differentiation of males among nine localities in continuous lowland habitats in Finland to the genetic differentiation among 14 localities in fragmented habitats in the Alps (France, Switzerland and Italy). In both areas, we found significant genetic differentiation. However, the average differentiation, measured as θ, was more than three times higher in the Alps than in Finland. The greater differentiation found in the Alps is probably due to the presence of mountain ridges rising above natural habitats of the species, which form barriers to gene flow, and to a higher influence of genetic drift resulting from lower effective sizes in highly fragmented habitats. The detection of isolation by distance in the Alps suggests that gene flow among populations does occur. The genetic variability measured as gene diversity HE and allelic richness A was lower in the Alps than in Finland. This could result from the higher fragmentation and/or from the fact that populations in the Alps are isolated from the main species range and have a lower effective size than in Finland. This study suggests that habitat fragmentation can affect genetic structure of avian species with relatively high dispersal propensities.

A molecular phylogeny of the Chalcidoidea (Hymenoptera).

Chalcidoidea (Hymenoptera) are extremely diverse with more than 23,000 species described and over 500,000 species estimated to exist. This is the first comprehensive phylogenetic analysis of the superfamily based on a molecular analysis of 18S and 28S ribosomal gene regions for 19 families, 72 subfamilies, 343 genera and 649 species. The 56 outgroups are comprised of Ceraphronoidea and most proctotrupomorph families, including Mymarommatidae. Data alignment and the impact of ambiguous regions are explored using a secondary structure analysis and automated (MAFFT) alignments of the core and pairing regions and regions of ambiguous alignment. Both likelihood and parsimony approaches are used to analyze the data. Overall there is no impact of alignment method, and few but substantial differences between likelihood and parsimony approaches. Monophyly of Chalcidoidea and a sister group relationship between Mymaridae and the remaining Chalcidoidea is strongly supported in all analyses. Either Mymarommatoidea or Diaprioidea are the sister group of Chalcidoidea depending on the analysis. Likelihood analyses place Rotoitidae as the sister group of the remaining Chalcidoidea after Mymaridae, whereas parsimony nests them within Chalcidoidea. Some traditional family groups are supported as monophyletic (Agaonidae, Eucharitidae, Encyrtidae, Eulophidae, Leucospidae, Mymaridae, Ormyridae, Signiphoridae, Tanaostigmatidae and Trichogrammatidae). Several other families are paraphyletic (Perilampidae) or polyphyletic (Aphelinidae, Chalcididae, Eupelmidae, Eurytomidae, Pteromalidae, Tetracampidae and Torymidae). Evolutionary scenarios discussed for Chalcidoidea include the evolution of phytophagy, egg parasitism, sternorrhynchan parasitism, hypermetamorphic development and heteronomy.