New Phytologist 210(3): 1107-1120 (May 2016)
Disruption of endosperm development is a major cause of hybrid seed inviability between Mimulus guttatus and M. nudatus.
Oneal, E, Willis, JH, Franks, R.

Summary

• Divergence of developmental mechanisms within populations may lead to hybrid developmental failure, and may be a factor driving speciation in angiosperms.

• We investigate patterns of endosperm and embryo development in Mimulus guttatus and the closely related, serpentine endemic M. nudatus, and compare them to those of reciprocal hybrid seed. We address whether disruption in hybrid seed development is the primary source of reproductive isolation between these sympatric taxa.

M. guttatus and M. nudatus differ in the pattern and timing of endosperm and embryo development. Some hybrid seed exhibit early disruption of endosperm development and are completely inviable, while others develop relatively normally at first, but later exhibit impaired endosperm proliferation and low germination success. These developmental patterns are reflected in mature hybrid seed, which are either small and flat (indicating little to no endosperm), or shriveled (indicating reduced endosperm volume). Hybrid seed inviability forms a potent reproductive barrier between M. guttatus and M. nudatus.

• We shed light on the extent of developmental variation between closely related species within the M. guttatus species complex, an important ecological model system, and provide a partial mechanism for the hybrid barrier between M. guttatus and M. nudatus.


Discussion

While hybrid seed lethality has long been recognized as a common postzygotic isolating mechanism among members of the ecologically and genetically diverse M. guttatus sp. complex (Vickery, 1978; Gardner and Macnair, 2000), our work is the first to provide a partial developmental mechanism—early arrested endosperm development and later failures of endosperm proliferation—for that outcome, and to provide insight into the early stages of endosperm and embryo development for members of the complex. We find that despite the fact that M. nudatus is likely recently derived from a M. guttatus‑like ancestor (Oneal et al., 2014), these species exhibit different patterns of embryo and endosperm development. The temporal coordination of development across cell types with different developmental roles is increasingly recognized as a critical aspect of achieving normal development (Del Toro-De León et al., 2014; Gillmor et al., 2014). We suggest that divergence in the timing of development between M. guttatus and M. nudatus may partly underlie the near complete hybrid barrier between them. Our work provides a framework for further investigation of the role of this fundamental developmental feature in the divergence between these closely related species. The extensive genomic tools already developed for the M. guttatus sp. complex, including an annotated genome sequence for M. guttatus, extensive Illumina re-sequence data from M. nudatus, and the continued development of transgenic experimental methods (Yuan et al., 2014) will only enhance future work on this important aspect of plant evolution and speciation.