Abstract
We now know that our bodies—and those of other invertebrate and vertebrate animals—are composed of networks of coupled circadian oscillators, veritable “clock shops” or “clockwork webs” of interacting tissues and organs (as termed by Herzog and Tosini, 2001, and Hastings et al., 2003, respectively). Neural, hormonal, and thermal signaling between central (brain) and peripheral (body) clocks enables organisms to set temporal programs that are individualized and adaptable.
But what about the situation in which the peripheral clock is actually an organism embodied within the host? A paradigmatic example is the intimate relationship between the little Hawaiian bobtail squid (Euprymna scolopes; Fig. 1) and its luminescent bacterial symbiont, Vibrio fischeri, a remarkable symbiosis that has been the focus of work by Margaret McFall-Ngai, Ned Ruby, and their associates for nearly 30 years (McFall-Ngai, 2014). The squid is a nocturnal hunter with a complex light organ that is believed to function as a generator of “counter illumination” for camouflage; that is, ventrally directed light serves to protect the squid from appearing to predators below as a dark silhouette against the water surface above (Jones and Nishiguchi, 2004). The light is produced by V. fischeri, which migrate from the seawater and inhabit the light organ. Light emission begins before sunset (Fig. 2), continues into the night, and after sunrise, the squid expels almost all of the bacteria and buries itself in the sand for its diurnal rest phase (Boettcher et al., 1996). At the level of the partners’ transcriptomes, interlocked rhythms time the changes in light organ anatomy with switches in bacterial metabolic pathways (Wier et al., 2010). But remarkably, luminescence of the bacteria directly influences the squid, rhythmically activating E. scolopes cryptochrome1 (escry1) gene expression in the light organ, implying that a local circadian oscillator in the host is sensitive to photic symbiont input (Heath-Heckman et al., 2013).
Intensities of light emission detected from juvenile E. scolopes maintained in a 12 h:12 h light-dark cycle. Each series of points represents an individual animal. Modified from Boettcher et al. (1996).
Of course, such a fascinating interplay is not restricted to invertebrates, and the 3 reviews in this issue of JBR highlight emerging insights and research on vertebrate, especially mammalian, systems. Xue Liang and Garret FitzGerald discuss microbial colonization of the gut, of intense interest given the association of compositional changes of the intestinal microbiome with a number of human diseases. Sarah Reece, Kimberley Prior, and Nicole Mideo consider the rhythmic intersection of parasites and their hosts, with important consequences for animal and human health and therapeutic interventions. Lastly, Peter Mark, Rachel Crew, Michaela Wharfe, and Brendan Waddell provide an update on the mechanisms and significance of maternal-fetal entrainment, including a view on the possible roles of the placenta. The embodied passengers in these examples can be viewed as peripheral oscillators, and they spur the typical questions—how are these oscillators entrained and what impact do their oscillations have for themselves and their hosts?
This is a truly integrative biology. Understanding the temporal coordination of physically locked clocks—whether between species or between generations within a species—is likely to impact, not only chronobiology but ecology, evolution, and developmental biology as well.