diversity Article Reproduction in Urbanised Coastal Waters: Shallow- Water Sea Anemones (Entacmaea quadricolor and Stichodactyla haddoni) Maintain High Genetic Diversity and Panmixia Wan Wen Rochelle Chan 1,*, Ywee Chieh Tay 1,2, Hui Ping Ang 3, Karenne Tun 3, Loke Ming Chou 1,2 , Danwei Huang 1,2,4 and Rudolf Meier 1,2 1 Department of Biological Sciences, National University of Singapore, 16 Science Drive 4, Singapore 117558, Singapore; [email protected] (Y.C.T.); [email protected] (L.M.C.); [email protected] (D.H.); [email protected] (R.M.) 2 Tropical Marine Science Institute, National University of Singapore, 18 Kent Ridge Road, Singapore 119227, Singapore 3 National Biodiversity Centre, National Parks Board, Singapore 259569, Singapore; [email protected] (H.P.A.); [email protected] (K.T.) 4 Centre for Nature-Based Climate Solutions, National University of Singapore, 16 Science Drive 4, Singapore 117558, Singapore * Correspondence: [email protected] Received: 11 August 2020; Accepted: 30 November 2020; Published: 8 December 2020 Abstract: Sea anemones are sedentary marine animals that tend to disperse via planktonic larvae and are predicted to have high population connectivity in undisturbed habitats. We test whether two sea anemone species living in two different tidal zones of a highly disturbed marine environment can maintain high genetic connectivity. More than 1000 loci with single-nucleotide polymorphisms (SNPs) were obtained with double-digest RADseq for 81 Stichodactyla haddoni and 99 Entacmaea quadricolor individuals to test for population genetic structure. We find evidence that both species predominantly propagate via sexual reproduction, and asexual reproduction is limited. We observe panmixia that indicates the absence of effective dispersal barriers for these species living in a highly anthropogenically disturbed environment. This is positive news for both species that are also found in the aquarium trade. More fundamentally, our results suggest that inhabiting different parts of a shallow reef may not affect a species’ population connectivity nor favour asexual reproduction. Keywords: fine-scale connectivity; ddRADseq; sea anemones; clonality 1. Introduction The construction of artificial coastal structures and increased shipping traffic can potentially interfere with the population connectivity of marine species and are thought to have negative effects on sedentary species with limited dispersal abilities [1,2]. Fortunately, many sedentary marine species have planktonic larvae that aid in dispersal [3–6] given that they can be transported over large distances via oceanic currents before settlement [6]. Broadcast spawning in anthozoans is considered the predominant method of reproduction, used in both hermaphroditic and gonochoric species [5]. The range of pelagic larval dispersal could be dependent on factors like the influence of currents (passive distribution for longer distances). However, short-distance dispersal of pelagic larvae has been speculated to be dependent on behaviour i.e., larvae remaining close to the benthos [7]. A good example of sedentary marine organisms that use broadcast spawning for maintaining panmixia are sea anemones (Cnidaria: Anthozoa: Actiniaria) [5], but how effective is this reproductive mode when living in heavily Diversity 2020, 12, 467; doi:10.3390/d12120467 www.mdpi.com/journal/diversity DiversityDiversity2020 2020, ,12 12,, 467 x FOR PEER REVIEW 2 2of of 18 18 example of sedentary marine organisms that use broadcast spawning for maintaining panmixia are impacted marine environments? Reduced genetic diversity [8,9] and population connectivity [10] have sea anemones (Cnidaria: Anthozoa: Actiniaria) [5], but how effective is this reproductive mode when been detected in populations settling on artificial structures. These are thought to be due to ecological living in heavily impacted marine environments? Reduced genetic diversity [8,9] and population and functional differences between natural and artificial structures and/or ‘phenotype-environment’ connectivity [10] have been detected in populations settling on artificial structures. These are thought unsuitability. Pollution in heavily impacted environments is furthermore known to cause mutations [11] to be due to ecological and functional differences between natural and artificial structures and/or with sublethal effects [12], which suggests that marine species in heavily disturbed environments could ‘phenotype-environment’ unsuitability. Pollution in heavily impacted environments is furthermore face a bleak future especially if the population connectivity is low. It would interfere with re-population known to cause mutations [11] with sublethal effects [12], which suggests that marine species in andheavily lower disturbed the capacity environments to recover could from disturbances.face a bleak future A decrease especially in the if the ability population of populations connectivity to adapt is tolow. rapidly It would changing interfere micro-conditions with re-population might occurand lower [13–15 the], given capacity that to higher recover genetic from diversity disturbances increases. A resiliencedecrease in of the populations ability of populations and the ecosystem to adapt toto rapidly disturbances changing [16– micro18]. Population-conditions might genetic occur data [13 also– allow15], given for reconstructing that higher genetic demographic diversity responses increases such resilience as effective of populations population and size, the genetic ecosystem diversity to anddisturbances migration [16 rates–18] to. Population contemporary genetic stressors. data also The allow data for could reconstructing thereforealso demographic inform conservation responses prioritisationsuch as effective and population management size, [19 genetic]. This isdiversity particularly and migration important rates for economically to contemporary important stressors. and endangeredThe data could species therefore [20–22]. also inform conservation prioritisation and management [19]. This is particularlySedentary important animals for such economically as sea anemones important have reproductiveand endangered strategies species that [20– are22] selected. to increase their chancesSedentary of survivalanimals [5such,23– 25as]. sea On anemones the one hand, have most reproductive species reproduce strategies sexually, that are which selected increases to theincrease genetic their diversity chances and of survival allows [ for5,23 adaptation–25]. On the in one dynamic hand, m andost species heterogeneous reproduce environments sexually, which [26 ]. Onincreases the other thehand, genetic asexual diversity modes and allow allows for quicklyfor adaptation reproducing in dynamic successful and genotypes heterogeneous that are well-adaptedenvironments to [26] prevailing. On the stable other andhand, homogeneous asexual modes environments allow for quickly [27,28]. Inreproducing sea anemones, successful sexual reproductiongenotypes that primarily are well involves-adapted broadcastto prevailing spawning stable and while homogeneous asexual reproduction environments may occur[27,28] by. In pedal sea laceration,anemones, longitudinal sexual reproduction fission or primarily transverse involves fission broadcast [29,30]. In spawning species with while a predominantlyasexual reproduction sexual modemay occu of reproduction,r by pedal laceration, highly connected longitudinal populations fission acrossor transverse different fission spatial [29,30] scales. andIn species higher with genetic a diversitypredominantly have been sexual observed mode of [31 reproduction,–33]. Conversely, highly species connected with asexualpopulations reproduction across different typically spatial show reducedscales and dispersal higher and genetic stronger diversity genetic have isolation been [observed34–37], because [31–33] individuals. Conversely, are species likely towith attach asexual to the firstreproduction hard surface typically that they show encounter reduced [38 dispersal]. and stronger genetic isolation [34–37], because individualsRecent observationalare likely to attach studies to the have first demonstratedhard surface that that they most encounter sea anemone [38]. species reproduce sexuallyRecent [5,23 observational,39–42]. For the studies sea anemone have demonstrateStichodactylad that haddoni most(Figure sea anemone1a), there species is no evidencereproduce of sexualsexually reproduction—asexuality [5,23,39–42]. For the sea appearsanemone to Stichodactyla be the main haddoni mode ( ofFigure reproduction 1a), there [is42 no]. Onevidence the other of hand,sexual sea reproduction anemones— likeasexualityEntacmaea appears quadricolor to be the(Figure main1b) mode [ 5,23 of] andreproductionS. gigantea [42][33. On] occasionally the other performhand, sea asexual anemones reproduction like Entacmaea via longitudinal quadricolor fission (Figure [23 ,130b), 43[5,].23] Unfortunately, and S. gigantea our [33] understanding occasionally of theperform reproductive asexual biologyreproduction of sea via anemones longitudinal is poor fission because [23,30,43 obtaining]. Unfortunately, high-quality our observational understanding data forof long-livedthe reproductive and slow-growing biology of sea anemones anemones is is time-consuming poor because obtaining [39,44]. Inhigh the-q marineuality observational environment, didatafficulties for long to directly-lived access,and slow track-growing and monitor anemones marine is speciestime-consuming in situ