How common is ecological speciation in plant-feeding insects? A 'Higher' Nematinae perspective

Abstract

Background: Ecological speciation is a process in which a transiently resource-polymorphic species divides into two specialized sister lineages as a result of divergent selection pressures caused by the use of multiple niches or environments. Ecology-based speciation has been studied intensively in plant-feeding insects, in which both sympatric and allopatric shifts onto novel host plants could speed up diversification. However, while numerous examples of species pairs likely to have originated by resource shifts have been found, the overall importance of ecological speciation in relation to other, non-ecological speciation modes remains unknown. Here, we apply phylogenetic information on sawflies belonging to the 'Higher' Nematinae (Hymenoptera: Tenthredinidae) to infer the frequency of niche shifts in relation to speciation events.

Results: Phylogenetic trees reconstructed on the basis of DNA sequence data show that the diversification of higher nematines has involved frequent shifts in larval feeding habits and in the use of plant taxa. However, the inferred number of resource shifts is considerably lower than the number of past speciation events, indicating that the majority of divergences have occurred by non-ecological allopatric speciation; based on a time-corrected analysis of sister species, we estimate that a maximum of c. 20% of lineage splits have been triggered by a change in resource use. In addition, we find that postspeciational changes in geographic distributions have led to broad sympatry in many species having identical host-plant ranges.

Conclusion: Our analysis indicates that the importance of niche shifts for the diversification of herbivorous insects is at present implicitly and explicitly overestimated. In the case of the Higher Nematinae, employing a time correction for sister-species comparisons lowered the proportion of apparent ecology-based speciation events from c. 50-60% to around 20%, but such corrections are still lacking in other herbivore groups. The observed convergent but asynchronous shifting among dominant northern plant taxa in many higher-nematine clades, in combination with the broad overlaps in the geographic distributions of numerous nematine species occupying near-identical niches, indicates that host-plant shifts and herbivore community assembly are largely unconstrained by direct or indirect competition among species. More phylogeny-based studies on connections between niche diversification and speciation are needed across many insect taxa, especially in groups that exhibit few host shifts in relation to speciation.

Figure 1

Phylogenetic distributions of host-plant taxa arising from different speciation modes in insects. (a) Distribution of host-plant taxa on the phylogeny of a hypothetical insect group in which speciation is mainly allopatric, and in which host shifts occur relatively infrequently in relation to speciation events. (b) Distribution of host taxa when speciation is mainly associated with host shifts. Note that only two host shifts are needed to explain current host-plant associations in a, whereas a minimum of six changes are needed to produce the pattern in b, although the number of speciation events is eight in both cases.

Figure 2

Examples of the diversity of resource use within the Higher Nematinae. (a) Female of Pristiphora mollis ovipositing on a leaf of Vaccinium myrtillus. (b) Larva of Amauronematus amplus feeding on Betula pubescens. (c) Colony of Pristiphora erichsonii larvae on Larix sp. (d) Larva of Phyllocolpa leucosticta inside opened leaf fold on Salix caprea. (e) Larva of Pristiphora angulata feeding on flowers of Spiraea chamaedryfolia. (f) Larva of Pontania pustulator inside opened leaf gall on Salix phylicifolia. (g) Melastola sp. larva inside opened berry of Vaccinium parvifolium. The locations of these exemplar species on the phylogeny of Higher Nematinae are indicated by letters in Fig. 3. (Photographs by T. Nyman).

Figure 3

Phylogeny of the Higher Nematinae and the diversification of host-plant use within the group. The tree was reconstructed according to a Bayesian phylogenetic analysis allowing a separate GTR+I+Γ₄ model of substitution for each gene. Numbers above branches show Bayesian posterior probabilities (%) followed by bootstrap proportions (%) from the corresponding ML analysis (hyphens in the place of bootstrap values denote clades that were not present in the ML tree). Branches are colored according to a maximum-parsimony reconstruction of host-family use, larval feeding habits are indicated by font colors and by symbols after species names (see legend). Species illustrated in Fig. 2 are indicated to the right of the tree.

Figure 4

Relaxed molecular-clock phylogeny of the Higher Nematinae, and the evolution of different larval habits within the group. The maximum clade credibility tree resulted from a topologically unconstrained Bayesian phylogenetic analysis employing a relaxed lognormal clock and a separate GTR+I+Γ₄ model of substitution for each gene. Numbers above branches show posterior probabilities (%), and blue shaded bars the 95% highest posterior density intervals for relative node ages for nodes with probabilities over 50%. Branch colors denote larval feeding habits according to unordered maximum-parsimony optimization, symbols to the right of species names show host-plant genera and families of the exemplar species (see legend). Full host ranges of polyphagous species are given in Additional file 1.

Figure 5

Distributions of Higher Nematinae species on different plant genera. Proportions are shown separately for the tribe Pristiphorini and for its sister clade composed of the tribes Mesoneurini and Nematini (see Figs. 3 and 4). Host data and estimates of species numbers are from Lacourt's [36] checklist of Western Palearctic sawflies, plant families are denoted by separate font colors (see legend). Numbers in parentheses after tribe names are in the order: total number of species/number of Western Palearctic species/number of Western Palearctic species with known hosts.

Figure 6

The probability that higher-nematine sister species have different niches in relation to time since their divergence. Data on pairwise niche differences (1 = different hosts and/or larval feeding habits; 0 = identical or overlapping niches) and split ages (= relative time since common ancestor) was taken from the 35 terminal sister-taxon pairs in the Bayesian MCC tree (Fig. 4), and the probability curve was estimated using logistic regression.