Transcriptomic signatures of population divergence in two
independent evolutionary lineages
We identified many genes differentially expressed between high- and
low-predation populations in each river drainage. The absolute number of
population DE transcripts was smaller in the Aripo drainage as compared
to the Quare drainage, but the number of developmental and interaction
differences was greater in the Aripo drainage. The Quare dataset was
1.5X larger than the Aripo dataset (40 versus 60 total samples) and the
identification of a greater number of DE genes in the Quare dataset is
therefore likely in part related to greater statistical power. This
difference may also be biological in origin, as high- and low-predation
populations in the Quare drainage show greater genetic divergence than
those in the Aripo drainage (Willing et al., 2010). Indeed, we note that
the larger number of genes in the Quare dataset come from a large
difference the number of genes with population, but not rearing or
interaction, effects. In sum, we suggest that the difference in the
number of differentially expressed transcripts between datasets is
likely a combination of greater statistical power in the larger Quare
dataset and the greater degree of genetic divergence in the Quare as
compared to the Aripo river drainage (Willing et al., 2010).
When we compared DE gene sets between drainages, we found a small, but
significant, number of population and rearing DE genes shared across
lineages. However, the majority of DE genes were non-shared across
drainages for both population (Aripo: 78%; Quare: 96%) and rearing
(Aripo: 94%; Quare: 92%) effects. Only rearing genes showed a
significant association in expression direction, with 67% of genes
concordantly differentially expressed between lineages. In contrast,
only 52% of the genes that diverged when low-predation fish colonized
high-predation habitats in both drainages were concordantly
differentially expressed. We suggest that these patterns across
drainages point to a small number of core genes that exhibit
predictable, plastic expression responses upon colonization of
low-predation environments, but that lineage-specific selection
pressures, differences in genetic background, non-adaptive processes
(e.g. drift, inbreeding, founder effects), and alternative compensatory
gene expression responses give rise to largely non-overlapping,
non-concordant expression differences associated with parallel
phenotypic adaptation across drainages.
A previous study in guppies performed a similar comparison of gene
expression changes associated with adaptation to low-predation
environments (Ghalambor et al., 2015) and found a strong signal of
concordant differential expression in genes differentially expressed
based on population of origin. Whereas the present study compared
long-term natural population divergence across drainages, Ghalambor et
al. (2015) characterized early stages of adaptation of experimentally
introduced low-predations populations derived from founders from a
single high-predation source population within the same drainage. These
contrasting findings in comparisons of population pairs within the same
drainage versus across drainages highlight the impacts of standing
genetic variation within the source population on mechanisms of
divergence (Feiner, Rago, While, & Uller, 2017; Thompson, Osmond, &
Schluter, 2019), particularly at early stages of evolution (Barrett &
Schluter, 2008): while alternative transcriptional ‘solutions’ are
possible, shared genetic background appears to bias evolutionary
outcomes toward shared patterns.
Both adaptive and non-adaptive processes may contribute to the
combination of shared and distinct transcriptional mechanisms we find
associated with parallel, adaptive life-history, morphological, and
behavioral phenotypes across lineages in guppies. First, as described
above, differences in standing genetic variation likely influence which
mechanisms are available to selection in response to common
environmental conditions in different drainages (Barrett & Schluter,
2008; Thompson et al., 2019). Second, low-predation populations are
typically established by a very small number of individuals (Barson et
al., 2009; Fraser et al., 2015; Willing et al., 2010), making them
susceptible to the unpredictable, non-adaptive influences of founder’s
effects, genetic drift, and/or inbreeding on gene expression divergence
– although we note that we found no more evidence for shared mechanisms
among genes most likely under selection than among all diverged genes
(i.e. genes with PST >
FST). Third, the large number of significantly evolved
genes that did not overlap between drainages may also represent adaptive
responses to drainage- or site-specific environmental factors other than
predation (Fitzpatrick, Torres-Dowdall, Reznick, Ghalambor, & Chris
Funk, 2014; Zandonà et al., 2011). Finally, alternative compensatory or
homeostatic gene expression responses may arise in response to any of
the above factors, leading to alternative transcriptional configurations
associated with similar higher-level phenotypes. In other words, genetic
similarity among ancestral populations may channel low-predation
populations within the same drainage toward shared transcriptional
solutions (as in Ghalambor et al. 2015), while differences in standing
genetic variation, drainage-specific environmental conditions, founder
effects, and alternative compensatory changes could result in distinct
mechanistic paths to arrive at shared organism-level phenotypes. We
cannot definitely distinguish causal from non-adaptive and compensatory
gene expression differences under these scenarios – indeed, it is
likely a combination of these factors that contribute to distinct
transcriptional patterns associated with parallel adaptation.
Nonetheless, in either case, alternative transcriptional patterns
suggest that mechanistic flexibility and ‘many-to-one’ mapping of gene
expression to organism level phenotypes may facilitate adaptation.