Extreme mitochondrial variation in the Atlantic gall crab Opecarcinus hypostegus (Decapoda: Cryptochiridae) reveals adaptive genetic divergence over Agaricia coral hosts

Abstract

The effectiveness of migration in marine species exhibiting a pelagic larval stage is determined by various factors, such as ocean currents, pelagic larval stage duration and active habitat selection. Direct measurement of larval movements is difficult and, consequently, factors determining the gene flow patterns remain poorly understood for many species. Patterns of gene flow play a key role in maintaining genetic homogeneity in a species by dampening the effects of local adaptation. Coral-dwelling gall crabs (Cryptochiridae) are obligate symbionts of stony corals (Scleractinia). Preliminary data showed high genetic diversity on the COI gene for 19 Opecarcinus hypostegus specimens collected off Curaçao. In this study, an additional 176 specimens were sequenced and used to characterize the population structure along the leeward side of Curaçao. Extremely high COI genetic variation was observed, with 146 polymorphic sites and 187 unique haplotypes. To determine the cause of this high genetic diversity, various gene flow scenarios (geographical distance along the coast, genetic partitioning over depth, and genetic differentiation by coral host) were examined. Adaptive genetic divergence across Agariciidae host species is suggested to be the main cause for the observed high intra-specific variance, hypothesised as early signs of speciation in O. hypostegus.

The stony coral Agaricia tenuifolia Dana, 1848 as a new gall crab host (Decapoda: Cryptochiridae)

“…10d, e). Moreover, no other cryptochirids are known to inhabit Agariciidae corals (van der Meij, 2014;Hoeksema et al, 2017;van Tienderen and van der Meij, 2017). A future effort to collect gall crabs from A. tenuifolia might be undertaken to confirm the crab's identity.…”

Highly polymorphic mitochondrial DNA and deceiving haplotypic differentiation: implications for assessing population genetic differentiation and connectivity

“…This species has a planktonic larval development (PLD unknown), with supposedly high potential for long-distance dispersal. Yet, gene flow in this species seems to be limited and follows an isolation-by-distance pattern [52]. Like M. neritoides , O. hypostegus shows an extreme degree of mtDNA COI variation ( Hd = 0.999; π = 0.026; 22% polymorphic sites; H p = 187 out of 195 specimens) [52].…”

“…Yet, gene flow in this species seems to be limited and follows an isolation-by-distance pattern [52]. Like M. neritoides , O. hypostegus shows an extreme degree of mtDNA COI variation ( Hd = 0.999; π = 0.026; 22% polymorphic sites; H p = 187 out of 195 specimens) [52]. This high mtDNA diversity was interpreted as an early sign of speciation resulting from adaptive genetic divergence over the coral host species.…”

“…This high mtDNA diversity was interpreted as an early sign of speciation resulting from adaptive genetic divergence over the coral host species. Yet, Fu and Li’s F and Tajima’s D were non-significant [52] and hence do not provide signal of selection and/or demographic expansion. Moreover, the nucleotide diversity at synonymous sites in O. hypostegus (calculated from [52]), is well-above the threshold of 5% ( π syn = 10.2%), indicating mtDNA hyperdiversity.…”

“…Yet, Fu and Li’s F and Tajima’s D were non-significant [52] and hence do not provide signal of selection and/or demographic expansion. Moreover, the nucleotide diversity at synonymous sites in O. hypostegus (calculated from [52]), is well-above the threshold of 5% ( π syn = 10.2%), indicating mtDNA hyperdiversity. This is in line with the bush-like pattern of the mtDNA haplotype network [Fig.…”