Multiple symbiont acquisition strategies as an adaptive mechanism in the coral Stylophora pistillata

Abstract

In obligate symbioses, the host's survival relies on the successful acquisition and maintenance of symbionts. Symbionts can either be transferred from parent to offspring via direct inheritance (vertical transmission) or acquired anew each generation from the environment (horizontal transmission). With vertical symbiont transmission, progeny benefit by not having to search for their obligate symbionts, and, with symbiont inheritance, a mechanism exists for perpetuating advantageous symbionts. But, if the progeny encounter an environment that differs from that of their parent, they may be disadvantaged if the inherited symbionts prove suboptimal. Conversely, while in horizontal symbiont acquisition host survival hinges on an unpredictable symbiont source, an individual host may acquire genetically diverse symbionts well suited to any given environment. In horizontal acquisition, however, a potentially advantageous symbiont will not be transmitted to subsequent generations. Adaptation in obligate symbioses may require mechanisms for both novel symbiont acquisition and symbiont inheritance. Using denaturing-gradient gel electrophoresis and real-time PCR, we identified the dinoflagellate symbionts (genus Symbiodinium) hosted by the Red Sea coral Stylophora pistillata throughout its ontogenesis and over depth. We present evidence that S. pistillata juvenile colonies may utilize both vertical and horizontal symbiont acquisition strategies. By releasing progeny with maternally derived symbionts, that are also capable of subsequent horizontal symbiont acquisition, coral colonies may acquire physiologically advantageous novel symbionts that are then perpetuated via vertical transmission to subsequent generations. With symbiont inheritance, natural selection can act upon the symbiotic variability, providing a mechanism for coral adaptation.

Figure 1. DGGE gel of Symbiodinium types present in Stylophora pistillata adults (Ad) and released planulae (Pl).

Samples were collected from both shallow (Sh, 2–6 m) and deep (Dp, 24–26 m) water. In all cases, the planula DGGE fingerprints were identical to that of their maternal colony. The sequence of the upper dominant band in the DGGE fingerprint from shallow water samples was identical to Symbiodinium type A1 (accession AF333505), while the lower dominant band showed a 1 bp difference from A1, indicating S. pistillata hosts an A1 variant. All deep-water samples hosted type C72 (accession AY765407). Symbiodinium A1 and C72 standards (Std) were run on every gel.

Figure 2. Schematic depicting potential scenarios (1–4) of symbiont inheritance and acquisition throughout Stylophora pistillata ontogenesis.

(1) Shallow water adults and planulae only host clade A Symbiodinium (•). Planulae settling in shallow water will become adults hosting clade A. (2) Some planulae from shallow water adults may settle in deep-water. These juveniles may horizontally acquire clade C Symbiodinium (+) while juveniles hosting only clade A may perish (×). (3) Deep-water adults abundantly host clade C Symbiodinium (potentially low-levels of clade A), and planulae only inherit clade C. Upon settlement in deep-water, juveniles will maintain clade C or horizontally acquire clade A. (4) Planulae from deep-water adults may settle in shallow water. Juveniles only hosting clade C may perish; horizontally acquiring clade A may facilitate survival to adulthood.