Maternal effects in coral fitness are reflected in gene
expression patterns
Maternal effects in recruit survival and size previously reported forA. loripes x A. tenuis hybrid corals were consistent with
their gene expression patterns. At the time when the corals were sampled
for gene expression analyses, hybrid LT and its maternal purebred LL had
higher survival compared to hybrid TL and its maternal purebred TT
(i.e., 36-49 % versus 7-23 %) under both ambient and elevated
conditions (Chan et al., 2018). Although the corals did not differ in
size at seven months of age, maternal effects on size were evident by
one year of age (Chan et al., 2018). In addition to the above study,
maternal effects have been reported in other Indo-PacificAcropora hybrid corals obtained via laboratory crossing. These
include effects on: 1) morphology of interspecific hybrids from anA. pulchra x A. millepora cross (Willis et al., 2006), 2)
survival of interspecific hybrid larvae from an A. florida xA. intermedia cross (Isomura et al., 2013), and 3) thermal
tolerance of intraspecific A. millepora hybrid larvae from a
higher and lower latitude population. In contrast, paternal effects were
found on morphology of natural interspecific hybrids of A.
palmata and A. cervicornis from the Caribbean (Vollmer &
Palumbi, 2002), and additive effects on survival (i.e., hybrid survival
was intermediate between the parental offspring) were observed in
experimentally produced intraspecific hybrids of A. milleporafrom a higher and lower latitude cross (van Oppen et al., 2014).
While a few studies have reported maternal effects on coral fitness and
morphology, little is known about maternal effects on gene expression.
In addition to the coral host, the host-associated microbiome can also
have an impact on host gene expression (Barfield et al., 2018; Helmkampf
et al., 2019). In our study, however, the bacterial and microalgal
endosymbiont communities of the corals were similar at the time of
sampling (Chan et al., 2019). The consistency between host gene
expression and phenotypic results thus suggests that maternal
host-related factors were likely the drivers behind the observed fitness
differences. Almost 2000 differentially expressed genes (DEGs) were
found when comparing hybrid LT and its maternal purebred LL to hybrid
TL, and maternal effects were evident in these corals based on PCA,
heatmap and volcano plots. While a statistical comparison cannot be made
back to the parental purebred TT due to small sample size, gene
expression of hybrid TL was similar to the only TT sample tested based
on PCA and the heatmap and was indicative of maternal effects.
Only a few studies have reported maternal effects in gene expression.
Videvall et al. (Videvall et al., 2016) showed that gene expression
patterns were distinct between parental populations of 12-week-old
seedling of the perennial herb Arabidopsis lyrata , and expression
in intraspecific hybrids was frequently more similar to that of the
maternal than paternal population. Only 15 DEGs were found between the
hybrid produced in one direction and its maternal population, yet
> 8800 DEGs were found when compared to its paternal
population (Videvall et al., 2016). Interestingly, maternal effects were
weaker in the hybrid cross of the other direction, with 334 and 661 DEGs
observed when compared to its maternal and paternal population
respectively (Videvall et al., 2016). Only one previous study has
examined maternal effects on coral hybrid gene expression and only coral
larvae were studied. Consistent with our findings, Dixon et al. (2015)
showed that gene expression of intraspecific A. millepora hybrid
larvae was similar to that of their maternal population. Up to 2,000
genes in hybrids were found to follow the expression patterns of the
maternal population (Dixon et al., 2015). In both studies however,
maternal effects were examined in early life stages only (i.e.,
12-week-old seedling and 6-day-old larvae). Our results show that
maternal effects can continue to influence gene expression of hybrid
corals up to the age of at least seven months, indicating the potential
long-term nature of maternal effects.
While differences in gene expression patterns were obvious between
reciprocal hybrids as well as between hybrid TL and its paternal
purebred, it was unclear what pathways and mechanisms were linked to
these differences. Gene ontology (GO) analyses revealed
underrepresentation of a very broad GO category, “cytosol”, in both
pairs of comparison, suggesting that a wide range of genes and pathways
were potentially involved in the observed holobiont fitness differences.
In contrast, clear pathways involved in maternal effects were observed
in the intraspecific A. millepora hybrid larvae (Dixon et al.,
2015). Analyses of cellular component categories of tolerance-associated
genes (i.e., genes for which expression levels prior to stress predicted
the probability of larval survival under stress) showed enrichment of
nuclear-encoded mitochondrial membrane components in hybrid coral larvae
whose parents come from a warmer latitude (Dixon et al., 2015). The most
upregulated GO categories were energy production and conversion, and
encompassed mitochondrial proteins, suggesting mitochondrial protein
variation in larvae may have contributed to maternal effects on thermal
tolerance (Dixon et al., 2015). In our study, however, no
mitochondrial-related pathways or genes were differentially expressed.
The difference in GO associated patterns between these two studies may
due to 1) the parental populations chosen for hybridization, and 2) the
symbiotic/aposymbiotic nature of the corals. Parental populations of the
same species from different latitudes were selected in Dixon et al.
(2015), whereas parental populations of two different species from the
same reef were chosen for this study. The differences in parental
thermal regimes in Dixon et al. (2015) may lead to clearer maternal
effects on thermal stress-related GO categories. Moreover, gene
expression responses of aposymbiotic larvae (in Dixon et al., 2015) were
likely different from coral recruits (in this study) that are associated
with a high density of microalgal endosymbionts. Hence, the contrasting
results of the two studies are unsurprising.