The Challenges of Optional Sex: the case of reproductive polyphenism in aphids
In last week’s colloquium, Gregory Davis illustrated the complexity of deciphering the mechanisms behind reproductive polyphenism using aphids as his model. Much of this work is available in his most recent review paper (Davis, 2012). He believes that such a novelty may have developed because an initial, slight change in morphology may have stimulated a modification of life history, with changes in life history feeding back to further changes in morphology, continuously playing off each other until obvious changes in body structure and development evolve.
Later in the season, as a reaction to the reduction in the photoperiod, the asexual females will start producing a new type of aphid: sexual females, who each produce haploid gametes with a single X chromosome, mate with males, and produce fertilized eggs that enter diapause and overwinter. This change in phenotype is associated with deep morphological changes: while sexuals are oviparous (they lay eggs), asexuals are viviparous (the embryos develop inside its mother) (see Figure 2, from Bickel et al., 2013). In asexual females, embryos develop within the ovaries, and even start reproducing themselves before being born!
Figure 1: Alternation of sexual and asexual phases in aphids.
Figure 2: Ovaries of sexual and asexual female pea aphids.
But what molecular pathway actually triggers the change in developmental fate? It has been previously observed that addition of juvenile hormone (JH) is sufficient to induce an asexual fate, even under the long photoperiod usually associated with sexual fate. JH is a hormone that regulates, among other things, the development of insects. It is particularly important for ensuring the full growth of larvae by preventing metamorphosis in the first couple of moltings (See Figure 3 for the classically described function of JH) (Corbit and Hardie 1985). To test the effect of the removal of JH, they used a plant derived compound, precocene, which acts by destroying cells of the corpora allatum, the endrocrine gland responsible for producing JH. However, interfering with JH has other consequences, such as the retention of juvenile characters and the interruption (called stalling) of the molting cycles at the 3rd instar. Indeed, asexual mothers exposed to long day photoperiods (which should therefore produce more asexual offspring) switched to producing sexuals when exposed to precocene (and also exhibited stalling). Interestingly, when applying precocene to sexual mothers exposed to short day photoperiods, no stalling effect could be detected in her offspring. Together these observations may suggest that it is embryonic levels of JH that are responsible for the specification of reproductive fate, rather than maternal levels of JH.
Figure 3: JH and molting phases in insects
Aphids are characterized for their “superfecundity”, or high reproductive capacity, resulting from the viviparous mechanism of asexual reproduction. Aphid response to the environmental cues, probably signaled through embryonic JH, allows the production of many individuals ready to spread during the optimum season while maintaining the advantages of sexual reproduction when weather becomes less ideal. Though the addition of an asexual phase for a sexual organism seems incredibly complex, Dr. Davis illustrated for us how such evolutionary transitions can be better understood by decoding the mechanisms behind such phenomena, increasing our understanding of how organisms can become so successful.
Bickel, RD; Cleveland, HC; Barkas, J; Jeschke, CC; Raz, AA; Stern, DL; Davis, GK. 2013. The pea aphid uses a version of the terminal system during oviparous, but not viviparous, development. EvoDevo, 4(1): 10. DOI:10.1186/2041-9139-4-10 (http://www.evodevojournal.com/content/4/1/10)
Corbit TS and Hardie J. 1985. Juvenile hormone effects on polymorphism in the pea aphid, Acyrthosiphon pisum. Entomologia Experimentalis et Applicata 38: 131-135.
Davis, GK. 2012. Cyclical Parthenogenesis and Viviparity in Aphids as Evolutionary Novelties. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 318(6): 448–459. DOI:10.1002/jez.b.22441 (http://onlinelibrary.wiley.com/doi/10.1002/jez.b.22441/abstract)
Ogawa K and Miura T. 2014. Aphid polyphenisms: trans-generational developmental regulation through viviparity. Front. Physiol. 5:1. doi: 10.3389/fphys.2014.00001
About Justin: Justin Rosenthal is a PhD. student working under Dr. Jian Wang and studies the genetic mechanisms of Drosophila nervous system development, specifically the rewiring of the learning centers during metamorphosis..