Changes in spawning time led to the speciation of the broadcast spawning corals Acropora digitifera and the cryptic species Acropora sp. 1 with similar gamete recognition systems

Abstract

Multi-species spawning is reported in the coral genus Acropora, but hybridization in nature rarely occurs because of the incompatibility of gametes and the timing of spawning. However, the evolutionary relationships between gamete compatibility and spawning time are obscure. Investigations of gamete compatibility in sister species that spawn at different times may provide clues to answering this question. Acropora sp. 1 has been defined as a cryptic species of Acropora digitifera, and they are morphologically similar, but spawn in different months, suggesting that they are either a cryptic species or a different species. We examined the morphology and conducted crossing experiments using cryopreserved sperm. The morphologies (branch length, branch width, and outer diameter of axial corallites) of A. digitifera and Acropora sp. 1 differed significantly. A phylogenetic tree of partial Pax-C nuclear sequences from A. digitifera and Acropora sp. 1 shows that they are monophyletic and closely related genetically, based on F ST values and P-distance. These results imply that these two species originated recently from a common ancestor. In addition, cryopreserved sperm from both A. digitifera and Acropora sp. 1 showed bidirectional inter-crossing (cryopreserved sperm of A. digitifera and eggs of Acropora sp. 1 from Sesoko: 32.1 ± 6.7 %, control-conspecific cryopreserved sperm and eggs: 46.1 ± 10.6 %; cryopreserved sperm of Acropora sp. 1 and eggs of A. digitifera from Oku: 63.3 ± 16.6 %, control: 83.6 ± 6.0 %). The results suggest that the gametes of these two species are compatible and that the pre-zygotic isolation mechanism is relaxed because their gametes do not interact. Overall, these two species should be classified as distinct species, and changes in spawning time are related to speciation in a similar gamete recognition system.

Spawning of <i>Acropora digitifera</i> in an aquarium as recorded by continuous interval photography using an underwater camera

“…The spawning timetable of A. digitifera at Sesoko Island in the present study and in Ohki et al (2015) correlates with previous reports on Acropora spawning in Japan: from 3 d before to 10 d after the full moon (see Fujiwara et al 2015, Mezaki 2016. Ohki et al (2015) reported that spawning of A. digitifera occurred on several days around the full moon of June, 2013 at the same locality as our study.…”

“…Ohki et al (2015) reported that spawning of A. digitifera occurred on several days around the full moon of June, 2013 at the same locality as our study. They observed the setting of gamete bundles at 20:30 hours to 21:00 hours to determine whether spawning had taken place.…”

“…Thus, previous observations on spawning of Acropora spp. (Fukami et al 2003, Ohki et al 2015, Zayasu & Shizato 2016) along with our aquarium data suggest the possibility that the peaks of bundle-like particle densitites after 00:00 (Fig. 2) are due to down-welling of bundles in the water column released between 22:00 hours to 00:00 hours.…”

Genetic differentiation and connectivity of morphological types of the broadcast‐spawning coral Galaxea fascicularis in the Nansei Islands, Japan

“…The octocoral species, Heliopora coerulea, is also separated into two genetic clusters that are related to branch morphotype (Yasuda et al 2014). Compared with G. fascicularis, these Acropora and Heliopora species are influenced by the difference in temporal reproductive isolation (Acropora: Hayashibara and Shimoike 2002;Ohki et al 2015;Heliopora: Villanueva 2015).…”

Phylogenomics provides new insight into evolutionary relationships and genealogical discordance in the reef-building coral genusAcropora

“…Acropora is the most speciose genus of hard corals, with 134 species [19] organized into 19 species groups based on skeletal similarities [20]. To date, molecular phylogenetic studies of Acropora have focused on the mitochondrial DNA Control Region (CR) and the nuclear PaxC intron [11,[21][22][23][24][25][26] (hereafter referred to as PaxC), which have produced significantly different phylogenies [11,22,27]. Incongruence between these regions has been attributed primarily to introgressive hybridization [11,22,23,27], but recent evidence suggests that PaxC is under selection and is associated with differences in spawning time, owing to two highly diverged PaxC lineages (F ST ¼ 0.98) that are correlated with different seasonal spawning cohorts in A. samoensis and A. tenuis [17,28].…”