Introduction
The order Gadiformes includes some of the most important commercial fish
(e.g., cod, hake, and haddock) in the world and accounts for
approximately 18% of the world’s total marine fish catch (FAO, 2004).
Gadiform fish inhabit cold waters in every high-latitude ocean from
deep-sea benthic habitats to coastal waters. Only two species in this
order are known in freshwater habitats (Nelson, 2006). However, to date,
only one high-quality genome sequence of the Gadiformes species, i.e.,
the Atlantic cod (Gadus morhua ) (Star et al., 2011), is
available, and this limitation significantly hinders the taxonomical,
evolutionary, and biological studies of the order Gadiformes.
The burbot Lota lota is the only member of the cod family
(Gadidae) that is adapted solely to freshwater (Schaefer et al., 2016).
This fish has a wide holarctic distribution, showing the widest
longitudinal range of freshwater fish in the world. The burbot is
distributed in nearly all suitable freshwater basins of North America,
Europe, and north Asia (Lehtonen, 1998). Although this fish thrives in
freshwater, L. lota has retained many characteristics of its
marine ancestors (Blabolil et al., 2018), such as preference for cold
water, spawning at low temperatures, high fecundity, and a pelagic
larval stage. This species spawns during winter or early spring,
typically when the water is still ice‐covered, and the water
temperatures are between 1 °C and 4 °C (Bergersen et al.,
1993).
Spawning occurs on fine to gravel substrate in shallow bays or groyne
fields in water depths of 0.3 m to 3.0 m (Fredrich &
Arzbach, 2002;
Eick et al., 2013).
The burbot is apparently an excellent “indicator” species. This
species is vulnerable to many environmental changes, in particular,
warming water temperatures and pollution (Stapanian et al., 2010). The
burbot in marginal habitats may serve as an early indicator of the
impacts of climate change on cold-water fish species (Stapanian et al.,
2010). However, stocks of the burbot have severely declined in number
and distribution during the past century. Many populations are
threatened, have been extirpated, or are otherwise in need of
conservation measures
(Maitland
& Lyle, 1990). For example, in Finland, burbot populations have
declined or have been destroyed completely in 16% of the lakes
(Tammi
et al., 1999). A series of threats, including pollution, habitat
fragmentation, exploitation, and invasive species, have caused the
decline or extirpation of many burbot populations (Stapanian et al.,
2010). Genomics resources will support the conservation studies of
burbot. Given the widest holarctic distribution of this species, the
burbot may undergo some degree of local adaptation, which can be
resolved with genome-wide high-quality SNPs. However, the available
genetic information for this fish remains scarce. At present, only
limited genetic studies have been conducted on the microsatellite loci
isolation and population structure of the burbot (Houdt et al., 2005;
Sanetra, 2005). Thus, sequencing the genome of the burbot is essential.
This process may help to reveal insights into the evolutionary history
of the burbot and the role of environmental changes in shaping the
genome evolution from marine to freshwater.
The burbot,the only freshwater species in the cod family
(Gadidae),represents a classical transition from marine to freshwater.
Fossil evidence suggests that the Lota genus has already
inhabited European rivers in the early Pliocene (Houdt et al., 2005).
This phenomenon indicates that the burbot left the ocean and migrated to
the freshwater. The transition from an oceanic to a freshwater habitat
provides an opportunity for drastic environmental changes in the
ecology, morphology, and behavior of fish. This transition should select
numerous functional genes. Marine to freshwater transition events rarely
occurs (Finnegan, 2017), which is likely due to physiological and
ecological barriers associated with changing environmental conditions.
These factors include lower salinity, relatively high levels of UV
radiation, dramatic fluctuations in freshwater temperature, and
competition from primary freshwater fish lineages. Despite these
challenges, several freshwater fish from marine-derived lineages have
completed this transition from ocean to freshwater and invaded
successfully freshwater habitats. Concerted effort, such as the
convergence of their morphological and physiological characters, has
been reported to freshwater adaptations (Jara, 1988). The genomic
changes underlying a convergent evolution may be reproducible to some
extent, and convergent phenotypic traits may commonly arise from the
same genetic changes. Physiological convergence is strong in freshwater
fish of marine-derived lineages and provides a practical way to identify
freshwater adaptations.
In this study, a chromosome-level genome assembly of burbot was
constructed by combining short reads, PacBio long reads, and Hi-C
sequencing data. The assembly was used to identify the genetic
signatures of evolution related to freshwater adaptation in burbot and
Perciformes by comparative genomics of 13 distantly related species,
including three freshwater Percomorpha species. This study will provide
a genomic resource to further address the key evolutionary process of
freshwater adaptation for marine-originated species.