Photoperiodic Diapause and the Establishment of Aedes albopictus (Diptera: Culicidae) in North America

Abstract

The invasion and range expansion of Aedes albopictus (Skuse) in North America represents an outstanding opportunity to study processes of invasion, range expansion, and climatic adaptation. Furthermore, knowledge obtained from such research is relevant to developing novel strategies to control this important vector species. Substantial evidence indicates that the photoperiodic diapause response is an important adaptation to climatic variation across the range of Ae. albopictus in North America. Photoperiodic diapause is a key determinant of abundance in both space and time, and the timing of entry into and exit out of diapause strongly affects seasonal population dynamics and thus the potential for arbovirus transmission. Emerging genomic technologies are making it possible to develop high-resolution, genome-wide genetic markers that can be used for genetic mapping of traits relevant to disease transmission and phylogeographic studies to elucidate invasion history. Recent work using next-generation sequencing technologies (e.g., RNA-seq), combined with physiological experiments, has provided extensive insight into the transcriptional basis of the diapause response in Ae. albopictus Applying this knowledge to identify novel targets for vector control represents an important future challenge. Finally, recent studies have begun to identify traits other than diapause that are affected by photoperiodism. Extending this work to identify additional traits influenced by photoperiod should produce important insights into the seasonal biology of Ae. albopictus.

Keywords: Aedes albopictus; adaptation; climate; diapause; photoperiodism.

Fig. 1.

Number of publications with “Aedes albopictus” in the title between 1970 and 2015 based on Pubmed search at http://www.ncbi.nlm.nih.gov/pubmed, accessed January 3, 2016. Note that this search is a conservative estimate of the number of studies concerning Aedes albopictus.

Fig. 2.

Effect of latitude and region (US = •, Japan = ○) in 1988 (A) and 2008 (B). 1988 data from Pumpuni (1989) and Focks et al. (1994). Results of ANCOVA in lower right of each panel indicate effects of Country, Latitude (Lat), and Country-by-Latitude interaction; ^***, P < 0.001; ^*, P < 0.05; ^ns, P > 0.05. Modified from Urbanski et al. (2012) with permission from the University of Chicago Press.

Fig. 3.

Experimental design of RNAseq studies to identify the transcriptional basis of diapause in Ae. albopictus during the stages of diapause induction, preparation, and developmental arrest (Huang et al. 2015; Poelchau et al. 2011, 2013a, 2013b). The transcriptomes of mosquitoes reared under diapause-inducing and nondiapause inducing photoperiods are compared at different developmental stages (adult females, stage V oocytes, embryos 72–78 h post oviposition, embryos 135–141 h post oviposition, and eggs 11, 21, and 40 d post oviposition).

Fig. 4.

Diagram of the citric acid (TCA) cycle, adapted from Ragland et al. (2010), illustrating gene expression changes between diapause (DI) and nondiapause (NDI) photoperiods for early (72–78 h) and late (135–141 h) stage embryos. Enzymes are depicted as rectangles, and metabolites as rounded rectangles. Significant fold-change values are depicted as shades of blue or yellow as indicated in the legend in the upper right; nonsignificant fold-change values are grey. Data from Poelchau et al. (2013b).

Fig. 5.

Log₂ fold change (FC) of the Ae. albopictus cyp18a1 orthologue under diapause (DI) vs. nondiapause (NDI) conditions at early embryological development (72–78 h), late embryological development (135–141 h), and 11 d, 21 d, and 40 d post oviposition. *** indicates P < 0.001, ns indicates P > 0.05. Data from Poelchau et al. (2013a, b).