4. Discussion
Genomic approaches are gaining importance in conservation biology. Lower
costs of sequencing and improvements in data analysis in non-model
organism has made these genetic tools more accessible. We present a
gold-standard draft genome of a NA blue whale assembled using integrated
second generation short-read and third generation long-read sequencing
data. The genome was used herein to discern for the first time the
population structure and demographic history of blue whales in the NA
using samples from present-day whales and whales collected in the early
1900’s through the 20th century, with the earliest
samples representing the blue whale population at the onset of
industrial whaling. Additionally, we investigated genes that appear to
be under positive selection in blue whales.
Our analysis of whole genome and mitochondrial DNA from present-day
(latitudes ~ 44°N to 79°N) and historic samples revealed
low population structuring among NA blue whales, indicating that the NA
blue whales comprise a single panmictic population. This is in contrast
to evidence gathered from satellite tracking and observational studies
(Lesage et al., 2017; Ramp & Sears, 2013, Silva et al., 2013), and
points to the complexities of studying large marine mammals in situ and
the importance of whole genome analyses to better understand population
structure. The full mitochondrial analysis suggests that the historical
samples from the South Atlantic and Antarctica are not as genetically
distinct from North Atlantic whales as nuclear DNA analyses suggest.
Further studies, with larger sample sizes, particularly for Antarctic
blue whales are needed including nuclear and mitochondrial DNA analyses
allowing us to test different aspects of population demography
We observed relatively high genome-wide heterozygosity in present-day NA
blue whales and one historical Antarctic whale sample, consistent with
reports of high heterozygosity observed in Chilean and other Antarctic
whales (Torres-Florez et al., 2014). Despite being hunted to the brink
of extinction, with the population size being reduced by more than 96%,
blue whales have retained high genetic variability. Thus, possible
long-term effects of severe bottlenecking may not be fully evident in
extant populations. High genetic diversity within the species is
promising for species recovery, if low population numbers do not persist
for an extended period of time. Similar high genetic diversity has been
observed in other species that have experienced extreme
overexploitation, such as Antarctic fur seals, but have since begun to
recover through conservation efforts (Paijmans et al., 2020). Our
examination of the demographic history of NA blue whales modeled on
genome wide heterozygous sites found a decline in blue whale numbers in
the North Atlantic over the last several hundreds of thousands of years
during multiple periods of glaciation. The PSMC methodology loses
resolution in relatively recent time periods and thus does not reveal
the impact of 19th and 20th century
whaling. Our results are similar to observations from an earlier study
by Árnason et al., (2018), although use of our blue whale de novoassembly allowed for a better estimation of the effective population
size at the end of the last glaciation providing an estimate of what the
NA blue whale population size may have been prior to whaling.
Blue and fin whales are the two largest animals on earth and can
hybridize even though they are not sibling species
(~8.35 million years since divergence) (Árnason et al.,
2018). Interspecific hybridization can occur naturally or result from
disruption of breeding due to anthropogenic effects. Hybridization with
introgression can in some cases lead to the extinction of distinct
species through swamping of the genome of one of the hybrid pairs. We
demonstrated gene flow between blue and fin whales in all of our
present-day and four (of six) historical samples; two whales from the
early 20th century lacked introgression. While our sample size is very
limited, this possible increase in the rate of introgression might be
related to reduced mate choice in blue whales due to their reduced
population size after industrial whaling. This hypothesis should be
further tested with larger sample sizes of whales from pre- and
post-whaling. The gene flow that we recorded between fin whales and NA
blue whales was not evident in previous studies (Árnason et al., 2018;
Westbury et al., 2019) that were done without the blue whale genome as a
reference. The direction of gene flow was fin to blue whale in all
present-day blue whales analyzed from NA, consistent with the
observation of several interspecific hybrids resulting from mating of a
male fin whales and female blue whales (Pampoulie et al., 2020).
We also assembled and annotated the NA blue whale transcriptome,
allowing for functional analysis of positively selected blue whale
genes. We identified several nAChR signaling pathway genes that are
associated with cancer development (Schuller, 2009) and also the
selection of genes involved in apoptosis. Earlier studies of suppression
of cancer in marine mammals detected positive selection of another
apoptosis pathway gene (ETNK1 ) in humpback whales (Tollis et al.,
2019) and positive selection of genes regulating nucleotide repair,
chromatin structure and transcription in bowhead whales (Keane et al.,
2015). Sperm whale gene analysis has revealed several cancer genes
(MMP7, CASP12 and PRSS33 ) that were positively selected
(Warren et al., 2017). Diseases like cancer which are associated with
age and large body size, surprisingly do not affect large aquatic
mammals (Keane et al., 2015; Tollis et al., 2019). The gene pathways
involved are not fully understood. Our analysis indicates functional
enrichment of genes in the nAChR pathway that might further elucidate
the underlying mechanism of cancer suppression. This might be a useful
tool in medical research.
In summary, the results from our study suggest that the blue whales in
the NA comprise a single population. Thus, future conservation
assessment and planning should be conducted in a holistic framework
viewing NA blue whales as a single population. Hybridization of blue
whales with fin whales is frequent in the NA and introgression might be
increasing in the present population. Future rates of introgression
should be monitored. The genetic variability in NA blue whales is high
and the slow recovery of blue whales in the NA is not associated with
reduction of heterozygosity via bottlenecking in extant populations.
However, it may become a factor in the future if populations do not
increase from their current low levels. Rates of introgression with fin
whales should be monitored. Further studies with a larger sample size
for present-day and historical blue whales from around the world could
be used to examine changes in levels of heterozygosity and resolve
questions regarding gene flow among populations of blue whales from
different oceans to enhance conservation planning efforts.