Research ArticleGENETICS

Large-scale diversification without genetic isolation in nematode symbionts of figs

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Science Advances  15 Jan 2016:
Vol. 2, no. 1, e1501031
DOI: 10.1126/sciadv.1501031
  • Fig. 1 Novelties and morphological diversity of nematode symbionts of figs.

    (A) Symbionts in the nematode genus Pristionchus are obligate associates of figs, such as F. sycomorus (shown here), in the African and Oriental tropics. (B) Fig-associated nematodes require transmission by pollinating wasps (Ceratosolen spp.), only a few of which are usually received by a given fig. (C and D) Two morphotypes (morphs I and II) of P. borbonicus, a symbiont of F. mauritiana. The beard-like labial morphology is a novelty known only for this species and P. sycomori. Scale bar, 10 μm. (E to I) Five alternative morphotypes of P. racemosae, a symbiont of the Australasian fig F. racemosa. Divergence of these morphs within species and with respect to the most closely related known fig associates is so great as to obscure homologies of traits or the morphs themselves. Scale bar, 20 μm.

  • Fig. 2 Genetic and phenotypic diversity in fig-associated Pristionchus nematodes.

    (A) Discrete adult morphs of P. borbonicus, P. sycomori, and P. racemosae. Homologous mouthpart regions are color-coded across morphs and species. (B) Projections of the first two principal components of mouth shape and form (PC1, principal component 1; PC2, principal component 2). Colors indicate morphs, as coded by labels in (A). Ovals represent a 95% confidence interval of the mean. (C) Genotype network for 49 individuals of P. borbonicus based on 10,500 single-nucleotide polymorphic sites. (D) Haplotype network for 77 individuals of P. sycomori based on sequences of ND1, Cytb, and COI genes. (E) Haplotype network for 104 individuals of P. racemosae based on sequences of the COI gene. (C to E) Each circle represents a unique genotype or haplotype and is colored according to morphs, as coded by labels in (A); if greater than 1, pairwise differences between joined haplotypes are denoted by hatch marks and vertices, with the latter also showing theoretical intermediate nodes introduced by the algorithm; the size of circles is proportional to the number of individuals sharing the same haplotype.

  • Fig. 3 Macroevolutionary disparity in fig symbionts relative to other Pristionchus species.

    (A) PCA of the mouth shape of 18 species of Pristionchus (PC1, principal component 1; PC2, principal component 2). Colors indicate morphs. (B) Phylogeny of Pristionchus spp. inferred from 18S and 28S rRNA genes and 27 ribosomal protein genes. Lineages that have radiated following a presumptively single fig colonization event are shown in green. Bars show disparity between morphs of selected polyphenic species, which was measured as maximal Euclidean pairwise distance in the morphospace between morph means. The color of bars is proportional to the number of morphs observed for a given fig-associated species. St, Eu, and Mg represent the two to three possible morphs in other Pristionchus species. Asterisk represents node support of 100% posterior probability.

  • Fig. 4 Conditional dependence and sexual dimorphism of morph production in individual figs.

    (A) Individuals of P. sycomori in figs shortly after pollination are exclusively of the microbivorous morph in both males and females. In later stages of fig development, concomitant with the increase in complexity especially attributable to the presence and action of other wasp-transmitted nematode species, subsequent generations of Pristionchus nematodes give rise to alternative morphs, including both of predatory and of novel unknown function. Each bar represents the morph ratio in a single fig, with males and females for that fig represented in corresponding columns. Columns for late interfloral phase figs, which were not separated further by age, are ordered by composition only. (B) Predation in different morphs of P. borbonicus. Normalized coverage of 18S rRNA genes of non-Pristionchus nematodes detected in genomes of 49 individuals of P. borbonicus is shown. Thin lines mark 0.25, 0.5, and 0.75 quantiles.

  • Fig. 5 Discrete morphs present in P. borbonicus (A to E) and P. sycomori (F to J).

    For both species, morphs are (from left to right) as follows: I, II, III, IV, and V. Scale bar, 20 μm.

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/2/1/e1501031/DC1

    Fig. S1. Positions of 13 two-dimensional landmarks recorded for the stoma of fig-associated Pristionchus species.

    Table S1. Nematode dauers transmitted by wasps (C. coecus) emerging from ripe figs of F. mauritiana.

    Table S2. Ratio of morphs in a single fig sycone for males and females of P. sycomori.

    Table S3. Nematode species isolated from sycones of F. mauritiana, F. sycomorus, and F. racemosa.

    Table S4. Proportion of variance explained by the first three principal component axes in the PCA of mouth form and shape for fig-associated Pristionchus species.

  • Supplementary Materials

    This PDF file includes:

    • Fig. S1. Positions of 13 two-dimensional landmarks recorded for the stoma of fig-associated Pristionchus species.
    • Table S1. Nematode dauers transmitted by wasps (C. coecus) emerging from ripe figs of F. mauritiana.
    • Table S2. Ratio of morphs in a single fig sycone for males and females of P. sycomori.
    • Table S3. Nematode species isolated from sycones of F. mauritiana, F. sycomorus, and F. racemosa.
    • Table S4. Proportion of variance explained by the first three principal component axes in the PCA of mouth form and shape for fig-associated Pristionchus species.

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