Depth-dependent parental effects create invisible barriers to coral dispersal

Abstract

Historically, marine populations were considered to be interconnected across large geographic regions due to the lack of apparent physical barriers to dispersal, coupled with a potentially widely dispersive pelagic larval stage. Recent studies, however, are providing increasing evidence of small-scale genetic segregation of populations across habitats and depths, separated in some cases by only a few dozen meters. Here, we performed a series of ex-situ and in-situ experiments using coral larvae of three brooding species from contrasting shallow- and deep-water reef habitats, and show that their settlement success, habitat choices, and subsequent survival are substantially influenced by parental effects in a habitat-dependent manner. Generally, larvae originating from deep-water corals, which experience less variable conditions, expressed more specific responses than shallow-water larvae, with a higher settlement success in simulated parental-habitat conditions. Survival of juvenile corals experimentally translocated to the sea was significantly lower when not at parental depths. We conclude that local adaptations and parental effects alongside larval selectivity and phenotype-environment mismatches combine to create invisible semipermeable barriers to coral dispersal and connectivity, leading to habitat-dependent population segregation.

Environmental specialization and cryptic genetic divergence in two massive coral species from the Florida Keys Reef Tract

“…This result is in agreement with that of Bongaerts et al (2017), where shallow‐to‐deep introgression in Agaricia fragilis is inferred from asymmetry in the private allele distribution, and Prada and Hellberg (2021), where asymmetrical introgression in the Caribbean octocoral Eunicea flexuosa is shown to favour the shallow‐to‐deep to direction. Moreover, it also aligns with recent experimental evidence from two Stylophora species and a brooding octocoral demonstrating that shallow‐origin larvae exhibit lower settlement specificity across shallow and deep conditions compared with mesophotic‐origin larvae (Shlesinger & Loya, 2021).…”

Plasticity of Porites astreoides Early Life History Stages Suggests Mesophotic Coral Ecosystems Act as Refugia in Bermuda

“…Importantly, the higher settlement success of mesophotic larvae under shallow light conditions compared to shallow larvae under mesophotic light conditions suggests that recruitment may preferentially occur up the slope (mesophotic to shallow) rather than down the slope (shallow to mesophotic). These results oppose previous observations of asymmetric gene flow (Prada and Hellberg, 2013;Serrano et al, 2014;Bongaerts et al, 2017) and larval settlement patterns (Shlesinger and Loya, 2021) occurring from shallow to deeper reefs. Nevertheless, the higher reproductive success observed for mesophotic corals in the Western Atlantic (Holstein et al, 2015; and subsequent larval effective recruitment found in the present study suggest that mesophotic reefs likely represent a significant source of propagules across the depth gradient and may aid in the recovery of degraded shallow reefs in Bermuda.…”

“…Furthermore, shallow reefs in Bermuda are more likely impacted by anthropogenic activities (Smith et al, 2013), which can also reduce the fitness of shallow adult colonies. Parental effects have been indicated as major factors limiting coral larval dispersal across depths as larvae may be adapted to the conditions experienced by their parent (Shlesinger and Loya, 2021), however, our findings show that offspring plasticity also plays a crucial role in shaping coral capacity to colonize differing environments. Yet, the density of adult P. astreoides colonies on shallow and mesophotic reefs in Bermuda does not reflect a pattern of increased recruitment to mesophotic depth, as adult colony frequency is documented to decrease with increasing depth (Fricke and Meischner, 1985).…”

“…Larval settlement is also documented to be driven in part by the benthic community, specifically the presence of crustose coralline algae (Morse et al, 1988;Ritson-Williams et al, 2009) and a bacterial film (Sneed et al, 2014). Shlesinger and Loya (2021) found that substrate type significantly influenced settlement choice by shallow and mesophotic larvae in the Red Sea, where larvae preferentially settled onto tiles conditioned at the corresponding depth of parental origin. Settlement tiles used in the present study, however, were all conditioned in a common garden environment on a nearshore shallow patch reef where conditions did not directly correspond to either site of parental origin, thereby reducing potential effects associated with tile conditioning.…”

In situ Estimation of Coral Recruitment Patterns From Shallow to Mesophotic Reefs Using an Optimized Fluorescence Imaging System

“…In mesophotic reefs, in situ surveys of recruitment patterns have mostly been limited to the northern Red Sea and Western Australia, where artificial settlement tiles have been employed to count new coral recruits (Turner et al, 2018;Kramer et al, 2019;Shlesinger and Loya, 2021). Several studies have evaluated in situ coral recruitment patterns in the shallow reefs of Eilat and Bermuda through visual underwater identification of coral recruits on settlement tiles or on the natural substrate (Smith, 1992;Glassom et al, 2004;Abelson et al, 2005;Glassom and Chadwick, 2006;Martinez and Abelson, 2013;Shlesinger and Loya, 2016;Guerrini et al, 2020).…”