Slight thermal stress exerts genetic diversity selection at coral (Acropora digitifera) larval stages

doi:10.21203/rs.3.rs-4941134/v1

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Slight thermal stress exerts genetic diversity selection at coral (Acropora digitifera) larval stages

https://doi.org/10.21203/rs.3.rs-4941134/v1

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Background

Rising seawater temperatures increasingly threaten coral reefs. The ability of coral larvae to withstand heat is crucial for maintaining reefs. While the reproductive process from spawning to larval dispersal is extensively studied, the influence of heat stress on genetic diversity at the individual larval level still needs to be clarified.

Results

This study investigates the larval response to heat stress before acquiring symbiotic algae, aiming to elucidate the relationship between coral genetic diversity and heat stress. Larvae sourced from eight Acropora digitifera colonies were subjected to ambient temperature (28°C) and heat conditions (31°C). The impact of heat stress on larval genetic diversity was assessed through sequencing. While overall genetic diversity, represented by π, did not significantly differ between the control and heat-exposed groups, Tajima’s D differed, indicating different selective pressures in each group. Twelve larval protein-coding sequences were identified on these loci, and the codon evolution of most of these genes showed signs of adaptive evolution. These results demonstrate the complex nature of the selective pressures operating in coral larvae under different temperatures, suggesting that corals might have experienced similar selection pressures during speciation.

Conclusion

These findings underscore the significance of genetic diversity in coral reproduction for maintaining reef ecosystems. They also indicate that even minor heat stress can exert significant selective pressure, potentially leading to profound implications for coral reef ecosystems. This research is crucial for understanding and mitigating the impact of rising seawater temperatures on coral reefs.

Coral reef ecosystems are rapidly declining owing to increasing mass bleaching [1]; successful larval recruitment following sexual reproduction is also decreasing [2]. Larval recruitment following sexual reproduction is a prerequisite for coral reef recovery and maintenance [3]. The reef-building coral Acropora spp. exhibits broadcast spawning, in which new larvae are generated from many conspecific colonies. The genetic diversity of spawned colonies influences the genetic diversity of the larvae [4]. Initially, these larvae do not have symbiotic algae and rely on their lipid reserves until they acquire symbiotic algae [5–7]. Once symbiotic relationships are established, the larvae receive energy assistance from the algae, disperse, and eventually settle [7, 8].

Before establishing a symbiotic relationship, the larval stage reflects the genetic characteristics of the parents, including heat tolerance [9]. Therefore, the genetic diversity of newborn coral larvae is associated with their survival under fluctuating water temperatures. Additionally, the water temperature influences the distance of larval dispersal [10–12]. However, which genotypes survive when exposed to high water temperatures, which can cause bleaching or lower survivorship (> 32 ^oC), has not been reported, and the degree of selection in the genome of each larva remains unknown.

The local adaptation of corals implies that genetic diversity is essential for adaptation [13–15]. Corals have experienced successive population declines, leading to genetic bottlenecks [13, 16, 17]. Although bottlenecks in heavy bleached populations have been predicted, a heterozygosity-based genetic perspective shows that their genetic diversity tends to recover within a short period [17, 18]. Gene flow has been observed among long-distance metapopulations during reef recovery [18–20]. This potential for rapid adaptation in coral populations provides hope for coral reef recovery. Therefore, elucidating changes in genetic diversity at the larval stages could enable us to understand how larvae adjust to warm conditions and how genetic diversity, resulting from synchronous spawning of many conspecific colonies, changes or is maintained for higher fitness.

Historically, coral reefs have undergone considerable environmental changes, including fluctuations in sea temperature [21, 22], which impose varying selective pressures on coral populations [22–24]. These historical selective pressures have shaped the genetic diversity observed in contemporary coral populations [13, 19], contributing to their adaptive potential [15, 24, 25]. Understanding how current environmental stressors, such as increased water temperatures due to climate change, affect the genetic diversity and selection patterns of coral larvae can provide insights into the evolutionary mechanisms that have enabled corals to survive environmental changes.

In this study, we combined genome-wide sequencing of individual coral larvae with proteomic analysis to identify the proteins present in the larvae. This dual approach allowed us to link the selective pressures observed at the genetic level to the proteins that constitute the larvae, providing a direct connection between the genotype and phenotype under heat stress conditions. This methodological innovation offers a comprehensive understanding of how genetic diversity and selective pressures shape the adaptive potential of coral larvae. However, this perspective has not been explored in previous studies. In this study, we aimed to investigate the impact of heat stress on genetic diversity and selective pressure in coral larvae, specifically examining how short-term exposure to elevated temperatures can influence genetic variation and selection patterns. By comparing the genetic responses of larvae exposed to control and heat stress conditions, we aimed to elucidate the potential for rapid adaptation and evolutionary significance of genetic diversity in coral populations.

Coral and larvae

Coral larvae were collected from eight Acropora digitifera colonies. Adult colonies were collected from the southern area of Sesoko Island (26.628989, 127.861517) and maintained under natural temperature (about 26 ^oC) and light conditions for 7 days before the full moon in May 2023. We checked whether the colonies had spawned by observing their settings and the appearance of gamete bundles at approximately 20:30. When colonies were set for spawning, each colony was transferred to a 10 L bucket. Spawning started at approximately 22:20, and bundles were collected and mixed from eight colonies (Fig. 1).

The larvae were maintained at approximately 27°C in buckets before the heat stress experiment. Three days post-spawning, larvae were exposed to different temperature regimes: control (26.8 ± 10.27°C, hourly mean ± SD) and heat (31.97 ± 0.19°C, hourly mean ± SD). Filtered fresh seawater (pore size 1 µm) was continuously supplied to each aquarium at a mean rate of 150 mL/min, with overflow for water change. In each treatment group, three aquariums (2 L) were housed with 200 larvae each (n = 600 larvae per treatment) for 21 days (Fig. 1). To avoid overcrowding, 100 larvae were divided into tubes (two tubes per aquarium), each covered with a filter to prevent the larvae from escaping. The control temperature was set at 27°C, reflecting the average sea-surface temperature during the experimental months, whereas the heat stress temperature was set to 31°C, the bleaching threshold for Acropora corals at the study location (Singh et al. 2019). Temperature elevation occurred gradually at a rate of 1°C per day, facilitated by a heater (Everes, Micro save power Heater 75 W, Tokyo, Japan) regulated by a temperature controller (Power Thermo ET-308; Kotobuki, Osaka, Japan). Light intensity was measured using a light quantum sensor (Biosphere Instrument Inc., Q5L 2100, San Diego, CA, USA) twice daily (09:00 and 16:00), ranging between 120 and 150 µmol m⁻²s⁻¹. To minimize light-induced variations, the aquarium positions within each treatment were rotated biweekly. A temperature logger (HOBO Pendant Temperature/Light K Data Logger) was used to monitor the seawater temperature hourly.

Parameter measurements

Mortality, motility, and metamorphosis were assessed to determine the effects of heat stress on the ability of the larvae to disperse and settle. Mortality was defined as the percentage of static or translucent larvae observed after 24 h. Careful inspection (20× magnification) ensured that the larvae did not metamorphose or attach to tube walls. Live larvae that were cigar-like or spherical in shape were scored for motility at 20× magnification. The fast-moving larvae were ranked as follows: static (but not translucent), 2. The mean motility ranks of the larvae in each tube were used as statistical replicates for each tank. Finally, metamorphosis was assessed as the percentage of larvae that formed flattened disks of tissue or single polyps (i.e., spats) that were attached to the walls of the tubes or were accessible in the water. Thus, each tank generated one replicate for mortality, motility, and metamorphosis each day when the incubations were completed.

Larval protein identification using LC-MS/MS

We identified proteins in 7 days post fertilization (dpf) coral larvae at ambient temperature (approximately 100 larvae) using LC-MS/MS, as described by M Morita, N Hanahara, MM Teramoto and AI Tarigan [26]. We used A. digitifera data from the NCBI database as reference information.

Genetic analyses to detect genetic diversity, selections, and codon evolution

Heat-exposed and control larvae were subjected to genome sequencing to examine the genetic diversity (π) and selective pressures (Tajima’s D) (Fig. 1). After experiments with control and heat-exposed larvae, larvae were kept in 99.5% ethanol and subjected to genome-wide amplicon sequencing, Gras-Di seq. The larvae were treated with lysis buffer (150 mM KCl, Tween-20 0.1 [W/V]%, Triton X-100 0.1 [W/V]%, Tris-HCl [8.0]) with 1 (µg/ml) proteinase K (nacarai tesque, Kyoto, Japan) for 2.5 h at 55 ^oC according to S Kitanobo, N Isomura, H Fukami, K Iwao and M Morita [27]. The supernatant, roughly having 50–200 ng/µL DNA, was used for the library preparation. We prepared a library according to M Furukawa, S Kitanobo, S Ohki, MM Teramoto, N Hanahara and M Morita [28]. Sequencing was conducted using a NovaSeq at Eurofin Co.

The single nucleotide polymorphisms of the larvae were isolated from the reference genome of A. digitifera. First, fastq files were cleaned with fatsp [29] and mapped onto the reference genome (Adig_2.0, GCA_014634965.1) using BWA-mem2 [30] and samtools [31]. The vcf files were output from the bam files with population.pl implemented in Stacks [32]. The vcf files were filtered with Plink according to Hardy–Weinberg equilibrium (--HWE 0.000001), minor allele frequency (--MAF 0.35), and calling rates (--geno 0.35). Filtered files were transformed back into VCF format to calculate genetic diversity using π and Tajima’s D with VCFtools. The window size was set to 100 bp due to the smaller scaffold size of the A. digitifera reference genome. Non-calling sites were eliminated, and the values of the control and heat-treated groups were compared. Loci with the highest and lowest 5 percentile Tajima’s D and π values were identified, focusing on higher values in either the control or heat-treated group. Loci with higher Tajima’s D values were regarded as signals of balancing selection, whereas those with lower values indicated positive selection. Using the Basic Local Alignment Search Tool (BLAST), 200-bp sequences were searched for before and after the loci with specifically high (95th percentile) or low (5th percentile) Tajima’s D values found only in the heat-treated or control groups. The best hit CDs were isolated, and those functions were searched for using KEGG or UniProt. The GO analyses could not be done due to the lack of GO terms registered in the NCBI gene bank database.

We then tested whether these genes underwent functional modifications during speciation. We examined the codon evolution of CDs using codeml in the PAML package [33] in the loci with higher or lower Tajima’s D values, representing balancing or positive selection, respectively. Model 8 is a positive selection model for nonsynonymous mutations, and Model 8a is a neutral evolution model for nonsynonymous and synonymous mutations. We ran the two models and conducted a likelihood ratio test of these two models. The orthologs of the CDs were isolated with an orthoscope [34], a phylogenetic tree was constructed with RaxML [35], and the analyses were run with tree and nucleotide files according to M Furukawa, S Kitanobo, S Ohki, MM Teramoto, N Hanahara and M Morita [28].

Statistics and reproducibility

Survival was plotted after Loess regression, and the Wilcoxon rank sum test was conducted to examine the differences between the control and heat conditions. Tajima’s D and π values were analyzed using the LMM with the lme4 and largest packages.

Larval survival in heat and control conditions

The survival rate of the heat-treated larvae was significantly lower than that of the control group, with approximately 50% and 70% survival in the heat-treated and control groups, respectively (Fig. 2a; LOESS correlation of three replicates with 95% confidence intervals shown in red or blue shadows. Wilcoxon rank sum test, P < 0.05).

Genetic diversity and selective pressures

Nucleotide diversity (π) was not significantly different between the control and heat-stressed groups, indicating similar levels of genetic variation (Fig. 2b; linear mixed model [LMM], AIC = -54829, logLik = 27418, Chisq = 1.107, df = 1, P > 0.05). In contrast, the difference in Tajima’s D values between the two groups was slight but significantly different, suggesting different selective pressures between the two groups (Fig. 2c; GLM, AIC = 17638, logLikelihood = -8814.9, df = 1, P < 0.01).

Loci under different types of selection

The loci under balancing selection (loci with high Tajima’s D values) and positive selection (loci with low Tajima’s D values) differed between the two groups (Fig. 3b, Table 1). In the heat-treated group, 9 and 13 coding sequences (CDs) were identified at the loci under balancing selection and positive selection, respectively (Supplementary Table 1). Under the control condition, 10 and 20 CDs were detected at these loci (Supplementary Table 1). For example, the loci in the 95th percentile of the highest values in the control and heat-treated groups differed. Several genes were identified at these loci (Supplementary Table 1).

Protein identification and functional annotation

Protein identification of coral larvae using liquid chromatography tandem mass spectroscopy (LC-MS/MS) indicated that some CDs encoded proteins in the larvae (Fig. 3a, Table 1). Most CDs are uncharacterized protein-encoding genes (“Others” in Fig. 3a); however, several are related to signal transduction (Genetic information processing; RNA splicing and second messenger-related), metabolism (response to oxygen levels), and Signaling and Receptors (actin binding, actin formation, and protocadherin) (Fig. 3a; Supplementary Table). Although the orthologues of some MS-identified proteins were not found with Orthoscope (Fig. 3b blue points), many of these CDs encoding larval and non-larval proteins were positively selected (Fig. 3b-red points with asterisks, Table 1, and Supplementary Table 1). For example, under thermal stress conditions, two RNA splicing-related enzymes, serine/arginine repetitive matrix protein 1, were under positive selection (Fig. 3b, Table 1). The lipid metabolism-related enzyme arylsulfatase-I predicted from UniProt was under positive and balancing selection conditions in heat-treated larvae (Fig. 3b, Table 1).

Complex selection pressures

Our codeml analysis revealed three genes on loci with high Tajima’s D values (indicative of balancing selection) in the heat-treated group, and two genes in the control group that exhibited signs of adaptive evolution (Table 1). In contrast, among the genes on loci with low Tajima’s D values (indicative of positive selection), only one of three genes in the heat-treated group and two of three genes in the control group exhibited adaptive evolution (Table 1). This gene also had a locus with high Tajima’s D value, suggesting that it is under complex selective pressures. Additionally, we examined codon evolution in non-larval protein-coding sequences and found that many of these sequences were undergoing adaptive evolution (Supplementary Table 1).

In this study, we examined how the genetic diversity of coral hosts changes in response to heat stress in larvae before they establish a symbiotic relationship. Genetic diversity resulting from sexual reproduction is crucial for the adaptability and long-term survival of populations and provides a reservoir for advantageous genetic variation under fluctuating water temperature conditions. Selective pressures, as indicated by Tajima’s D values, differed between the control and heat stress groups, whereas nucleotide diversity (π) did not differ significantly. This suggests that thermal stress can rapidly influence selective pressure on larvae from the time of spawning, leading to adaptation.

The selective pressure on coral larvae varied significantly with water temperature over a short period, leading to differences in the genes on loci with higher Tajima’s D values between the control and heat stress groups. These findings highlighted the importance of genetic diversity in newborn larvae. The number of colonies that participate in synchronous spawning affects the genetic diversity of subsequent generations. In other words, promiscuous fertilization of colonies results in diverse larvae, and changes in genetic diversity at the larval stage might indicate natural selection. Notably, bleaching events reduce the number of released gametes owing to a decline in colony numbers [36] and decline in gamete production [37], potentially accelerating the decrease in the genetic diversity of coral larvae.

Balancing selection occurs in the co-chaperone sacsin and might result in thermal tolerance [13]. Therefore, the number of colonies contributing to spawning and the number of gametes are associated with the amount and genetic diversity of the larvae. In contrast, thermal stress influences gamete production [37], and thus, reproductive states are difficult to determine only from the colony numbers in the reef. Although slight changes in water temperature influence the genetic diversity of the larvae, heat-stressed larvae might not form a strikingly heat-tolerant colony. The diversity of the new generation might be affected by fluctuations in water temperature; thus, diversity might be profitable for survival in unexpected water temperatures. Further long-term monitoring experiments from larval to adult colonies are required.

Our individual larvae sequencing revealed that the surviving larvae had specific genetically divergent loci, particularly those related to lipid metabolism and ontogenic processes, and were larva-composing proteins. Although we identified the proteins in the 7 dpf larvae of the only control condition, this finding is significant because lipids are crucial for coral larval metabolism prior to symbiont acquisition. Notably, the metabolic rates of lipids are rapid in non-symbiotic larvae [7], further highlighting the role of lipid metabolism in the survival of coral larvae under heat stress. The expression of arylsulfatase, related to lipid metabolism, which was analyzed under balancing and positive selection in this study, was previously found to increase in oyster larvae with ocean acidification [38]. In contrast, lipid depletion did not affect larval survival under heat stress [39]. The loci in the heat-treated group were divergent from those in the control group, suggesting balancing selection at specific loci, leading to potential adaptation to heat stress. However, the genetic divergence of the enzymes involved in lipid metabolism has yet to be clarified, as they are associated with lipid consumption and heat tolerance.

Balancing and positive selection, according to Tajima’s D values, implied that complex selective pressures worked at the larval stages. Balancing selection is related to bleaching resistance [13], and loci with higher Tajima’s D values often match with higher genetically divergent loci, represented by higher Fst values [22]. Genetic divergence among species is often accompanied by evolution [28]. These alignments are well explained by CDs in the loci with higher Tajima’s D values, which are under positive selection of codons (Table 1). In contrast, arylsulfatase 1-like is on loci with both higher and lower Tajima’s D values, showing adaptive codon evolution, representing the complex history of the reef-building coral Acropora spp. during speciation accompanied by sea level changes [21]. This dual selection mechanism suggests that coral larvae maintain a flexible and adaptive genetic repertoire essential for survival in changing environments. Our study underscores the importance of genetic diversity in sexual reproduction as a reservoir of adaptive potential, which is crucial for populations facing fluctuating environmental conditions.

The heat stress response in the coral occurs via complex interactions between the host and holobionts; however, we only focused on aposymbiotic larvae to examine the selection of heat stress on the host genome. Selection can be performed after fertilization until a symbiotic relationship is established. The larvae from heat-tolerant colonies were more tolerant or unrelated to non-Acropora corals [19, 40]. This contradiction is plausible to represent the complex heat tolerance mechanisms, from symbiotic algae to host [41].

This study indicates that a mixture of positive and balancing selections due to heat stress potentially occurs from fertilization to symbiotic larvae but does not clearly show the linkage between these selections and adaptations. Notably, we used the June-spawning species A. digitifera, which is not exposed to severe heat stress during its larval dispersal because its spawning month is during the rainy season in Okinawa, Japan. However, on sunny days, the seawater surface temperature reached high temperatures, which is during the larval dispersal stage from June to July [42]. Although the effect of water temperature on the larvae until a symbiotic relationship is formed is unknown, larvae from the sexual reproduction stage can arise from a mixture of many synchronous spawning colonies. In other words, selection could operate in larvae; in turn, larvae with high genetic divergence are potentially profitable in their subsequent life stages, such as survival until reproduction, leading to higher fitness of the following colonies [43]. This is a typical benefit of sexual reproduction, representing the Fisher–Müller effect [44]. This study describes this phenomenon, representing sexual reproduction in the synchronous broadcast-spawning coral Acropora spp.

These findings have significant implications for coral reef conservation. Although we identified specific genetic loci under selections, we have yet to confirm corresponding proteins that enhance heat tolerance. However, breeding programs have aimed at producing heat-resistant coral strains [3, 45, 46]. High genetic diversity provides a reservoir of adaptive traits, increasing the likelihood of some colonies surviving warm conditions [19]. However, sexual reproduction is essential for generating this genetic diversity and successive heat waves have complicated reef recovery [47, 48]. Additionally, epigenetic responses, such as memory of thermal stress, are related to thermal acclimation [49]. The gap between adaptation via genetic diversity and the complex mechanisms that confer adaptation to nature requires further investigation.

Nevertheless, this study highlights the integration of genomic and proteomic analyses to uncover the genetic and phenotypic bases of heat tolerance in coral larvae. By combining cutting-edge methodologies with practical conservation applications, this study represents a significant advancement in the fields of coral biology and climate change adaptation. Our findings emphasize the importance of maintaining genetic diversity for the adaptive potential and long-term survival of coral populations and offer valuable insights into coral reef conservation in the face of global climate change.

Acknowledgments

We thank Professor Shunichi Takahashi for supporting us with the thermal aquarium setup and the technical staff of the Sesoko Marine Station, University of the Ryukyus, for supporting us with fieldwork.

Funding: This work was partly supported by JSPS KAKENHI (17K07414, 21H05304, and 22H02369 to MM).

Author contributions: CM and AIT performed larval aquarium experiments; YA collected larval samples for LC-MS/MS analyses; NH performed bioinformatics analyses; MF supported to conduct DNA extraction; MM conceived the study design, performed informatics and molecular evolutionary analyses, and wrote the paper. All authors contributed critically to drafts and approved the final manuscript for publication.

Competing interests: All other authors declare they have no competing interests.

Data and materials availability: All data are available in the main text or supplementary materials. The sequence data were shared in GenBank, and the scripts for the analyses were shared in GitHub (https://github.com/Masaya0606/Aditifera_larvae).

Ethics approval and consent to participate: Not applicable

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Table 1 is available in the Supplementary Files section.

No competing interests reported.

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Slight thermal stress exerts genetic diversity selection at coral (Acropora digitifera) larval stages

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Abstract

Figures

Introduction

Methods

Coral and larvae

Parameter measurements

Larval protein identification using LC-MS/MS

Genetic analyses to detect genetic diversity, selections, and codon evolution

Statistics and reproducibility

Results

Larval survival in heat and control conditions

Genetic diversity and selective pressures

Loci under different types of selection

Protein identification and functional annotation

Complex selection pressures

Discussion

Declarations

References

Table

Additional Declarations

Supplementary Files

Status:

Version 1