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 (Table 1) were
consistent with their gene expression patterns. At the time when the
corals were sampled for gene expression analyses, the hybrid LT and its
maternal purebred LL had higher survival compared to the hybrid TL and
its maternal purebred TT under both ambient and elevated conditions.
Although the corals did not differ in size at seven months of age,
maternal effects in size were evident by one year of age (Table 1).
Maternal effects have previously been reported for other Indo-PacificAcropora hybrid corals obtained via laboratory crossing. These
include effects in: 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 in morphology of natural interspecific hybrids of A.
palmata and A. cervicornis from the Caribbean (Vollmer &
Palumbi, 2002), and additive effects in 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 in coral fitness and
morphology, little is known about maternal effects in 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; Buerger
et al., 2020; Helmkampf et al., 2019). In our study, however, the
bacterial and microalgal endosymbiont communities of the corals were
similar at the time of sampling (Table 1). 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. A large number of differentially expressed genes
(~2000 DEGs) were found when comparing offspring groups
that had different maternal parent species (i.e., between the hybrid TL
and its paternal purebred LL, and between the reciprocal hybrids), but
not when the groups shared the same maternal parent species (i.e., only
40 DEGs between the hybrid LT and its maternal purebred LL). 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
was indicative of maternal effects. The four samples omitted from the
main analyses because of their small library sizes also supported the
presence of maternal effects, although inferences drawn from these
samples should be taken with caution.
In our study, however, no mitochondrial genes were differentially
expressed and PCA and heatmap of mitochondrial genes did not show
maternal patterns. In other words, evidence of maternal gene expression
patterns was only found in the nuclear genes, but not in the
mitochondrial genes or via mito-nuclear crosstalk in this study
(although note that only seven mitochondrial genes were available for
comparison post-filtering).
Several studies have reported maternal effects in gene expression
including in a perennial herb (Videvall et al., 2016), coral (Dixon et
al., 2015), pipefish (Beemelmanns & Roth, 2016) and stickleback
(Metzger & Schulte, 2016; Mommer & Bell, 2014; Shama et al., 2016),
and maternal environments have also been demonstrated to affect DNA
methylation of sea urchin (Strader et al., 2020). Videvall et al. (2016)
showed that gene expression patterns were distinct between parental
populations of 12-week-old seedling of the perennial herbArabidopsis 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 in 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 (i.e., up to 2,000 genes in hybrids followed
the expression patterns of the maternal population). In these studies
(Dixon et al., 2015 and Videvall et al., 2016) 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 the hybrid TL and its paternal
purebred, it was unclear what pathways and mechanisms were linked to
these differences and underpinned observed phenotypic differences (Chan
et al., 2018). Gene ontology (GO) analyses revealed underrepresentation
of a very broad GO category, “cytosol”, in both pairs of comparison.
It is also possible that maternal provisioning had long-lasting effects
in offspring (that were seven months old) and was responsible for the
phenotypic and gene expression differences (i.e., poorly provisioned
offspring may exhibit pervasive differences in transcription). Future
studies on maternal effects in corals will benefit from quantifying
differences in maternal provisioning between the parental species, such
as lipid/protein content of eggs and early larvae.
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 in thermal
tolerance (Dixon et al., 2015).
The difference in GO associated patterns between these two studies may
be due to 1) the parental populations chosen for hybridization, 2) the
symbiotic/aposymbiotic nature of the corals and 3) the life stage 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 in 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 were associated with a high density of microalgal
endosymbionts. The effects of maternal provisioning on gene expression
is also likely to be stronger in early larvae than in seven-month-old
recruits. Hence, the contrasting results of the two studies are
unsurprising. Further, mitochondrial genes may not show maternal
patterns if maternal provisioning was responsible for the phenotypic
maternal patterns observed in these corals.