Convergent evolution of saccate body shapes in nematodes through distinct developmental mechanisms.

BACKGROUND

The vast majority of nematode species have vermiform (worm-shaped) body plans throughout post-embryonic development. However, atypical body shapes have evolved multiple times. The plant-parasitic Tylenchomorpha nematode hatches as a vermiform infective juvenile. Following infection and the establishment of a feeding site, grows disproportionately greater in width than length, developing into a saccate adult. Body size in was previously shown to correlate with post-embryonic divisions of laterally positioned stem cell-like 'seam' cells and endoreduplication of seam cell epidermal daughters. To test if a similar mechanism produces the unusual body shape of saccate parasitic nematodes, we compared seam cell development and epidermal ploidy levels of to . To study the evolution of body shape development, we examined seam cell development of four additional Tylenchomorpha species with vermiform or saccate body shapes.

RESULTS

We confirmed the presence of seam cell homologs and their proliferation in . This results in the adult female epidermis having approximately 1800 nuclei compared with the 139 nuclei in the primary epidermal syncytium of . Similar to we found a significant correlation between body volume and the number and ploidy level of epidermal nuclei. While we found that the seam cells also proliferate in the independently evolved saccate nematode following infection, the division pattern differed substantially from that seen in . Interestingly, the close relative of does not undergo extensive seam cell proliferation during its development into a saccate form.

CONCLUSIONS

Our data reveal that seam cell proliferation and epidermal nuclear ploidy correlate with growth in . Our finding of distinct seam cell division patterns in the independently evolved saccate species and is suggestive of parallel evolution of saccate forms. The lack of seam cell proliferation in demonstrates that seam cell proliferation and endoreduplication are not strictly required for increased body volume and atypical body shape. We speculate that may serve as an extant transitional model for the evolution of saccate body shape.