Discussion
Identifying global patterns in genetic diversity is a fundamental goal
in ecology and evolution. Since genetic diversity is a proxy for
adaptive potential and the raw material for speciation events,
determining its spatial distribution can help us better understand which
species are most vulnerable to anthropogenic change and help explain
global patterns in species diversity. Here, we outlined and tested three
distinct macroecological drivers of intraspecific genetic diversity,
identified global patterns, and assessed the congruence of these
relationships across the genome. Overall, we found that nuclear genetic
diversity was most strongly correlated with chlorophyll-a concentration,
a proxy for primary productivity and resource availability, while
mitochondrial diversity was tightly associated with chlorophyll-a
concentration, sea surface temperature, latitude, and longitude. Taken
together, these results provide support for our original hypotheses to
varying degrees. The quadratic relationship between chlorophyll-a
concentration and genetic diversity across the genome provides
compelling evidence for the Productivity-Diversity Hypothesis and
suggests that regions of higher productivity facilitate larger
population sizes, and in turn, higher levels of genetic variation.
However, our results suggest a tipping point may exist in this
relationship, after which larger carrying capacities may result in
reduced population sizes and declining genetic diversity (Lawrence &
Fraser, 2020). Furthermore, temperature was positively correlated with
mitochondrial genetic diversity, lending support to the Kinetic Energy
Hypothesis and the relationship between temperature, metabolism, and
mutation rates. The lack of a significant correlation with nuclear
diversity further affirmed this theory, as oxidative damage is not
expected to impact nuclear DNA and increase nuclear mutation rates in
the same manner (Hoffman et al. 2004).
Interestingly, the Founder Effect Hypothesis was the only one of our
three initial hypotheses the three that we did not find full support
for, although the observed decline in mitochondrial genetic diversity
towards the poles is in line with the hypothesis’ predictions. This
decline was particularly pronounced near the Arctic, congruent with the
outsized impact of glacial expansion on Northern hemisphere species,
relative to their Southern Ocean counterparts (Fraser et al. 2012).
Furthermore, the smaller Ne of mitochondrial DNA
makes it more sensitive to LGM-induced bottlenecks (Birkey et al. 1989);
strengthening any LGM signal in mitochondrial genetic diversity.
Alternatively, the high levels of dispersal and admixture often observed
in marine systems, along with high Ne s, may
explain why a poleward decline was not observed in nuclear diversity, as
elevated dispersal across the species range may help transport genetic
diversity from the center to the poleward edge and replenish depleted
gene pools. In fact, many temperate marine species harbor consistent
levels of genetic diversity across their species range (Almada et al.
2012; Francisco et al. 2014; Martínez et al. 2015). Furthermore,
microrefugia during the LGM that are uncoupled from historical climatic
gradients may provide “re-seeding” opportunities for formerly
glaciated regions and help buffer northern populations from extirpation,
similar to previously documented patterns in the Antarctic (Suggitt et
al. 2018). Given that some of these past refugia are close to modern
northern range limits, expansion waves out of these locations would have
been less susceptible to diversity loss from bottlenecks or serial
founder events (Bringloe et al. 2020; Maggs et al. 2008).
Previous studies have also found latitudinal gradients in mitochondrial
genetic diversity, including Manel et al. (2020), another prominent
macrogenetic study that analyzed global patterns in marine fish genetic
diversity. However, the methods and statistical analyses frequently
employed by macrogenetic studies have come under recent criticism
(Gratton et al. 2017, Paz-Vinas et al. 2021). Most earlier macrogenetic
studies fall into the category of Class III (Leigh et al. 2021) -
pooling samples and sequences into predefined grid cells or latitudinal
bands, calculating diversity at the species level, then averaging all
species estimates together (Manel et al. 2020; Miraldo et al. 2016;
Theodoridis et al. 2020). While informative, studies of this design
often fail to account for genetic variation within species (such as from
the range center to edge), for the relative frequency of individual
haplotypes within each population, for study-specific methodological
choices, or for the unbalanced sampling of species across grid cells
(Gratton et al. 2017; Paz-Vinas et al. 2021). As population size is the
mediating factor in many hypotheses aimed at explaining global patterns
of genetic diversity, including those assessed here, such distinctions
are important. Genetic diversity may follow different spatial patterns
at different scales, given that environmental gradients, ecosystem
processes, and biogeography collectively influence how population-level
genetic diversity is shaped into community-wide patterns (De Kort et al.
2021). Here, we conducted a Class II macrogenetic study, which enabled
us to incorporate metadata from the original populations, including
sample sizes and the demarcation of local populations (Leigh et al.
2021). This approach enabled us to better account for issues of
within-species geographic variation and relative haplotype abundance.
Despite these differing techniques, our findings also show that
mitochondrial diversity follows clear latitudinal and longitudinal
gradients - peaking at lower latitudes and in the Indo-Pacific - and
reaffirm patterns previously established in Manel et al. (2020).
Interestingly, the Coral Triangle has been designated as the center of
species biodiversity, and our models suggest it could play a similar
role for genetic diversity, especially within the mitochondria. These
results are unsurprising, as several of the predictors we found to be
strongly associated with mitochondrial diversity (e.g. sea surface
temperature) have also been linked with higher species richness
(Tittensor et al. 2010). Furthermore, heightened habitat availability
and coastline length have been suggested as specific drivers of species
richness in the Coral Triangle and could also increase genetic diversity
through their positive influence on population size (Sanciangco et al.
2013). However, our models suggest that other regions in the
Indo-Pacific show elevated mitochondrial genetic diversity as well,
including the coastline of the Indian subcontinent and Sri Lanka,
suggesting other macroecological factors may also play an important role
in creating and maintaining genetic diversity.
Importantly, compared to mitochondrial diversity, nuclear genetic
diversity did not follow clear geographic gradients across either
latitude or longitude. These results are similar to previous studies
that saw no strong latitudinal patterns in the nuclear diversity of
mammals (Schmidt et al. 2022), freshwater fish (Lawrence et al. 2023),
plants (De Kort et al. 2021), or habitat-forming species
(Figuerola-Ferrando et al. 2023). As nuclear diversity is more tightly
coupled with population size than is mitochondrial diversity (Bazin et
al. 2006), recent demographic processes or changes in population size
may disrupt any pre-existing geographic patterns and result in no clear
latitudinal gradients in diversity. When compared to the spatial
gradients in mitochondrial genetic diversity, the inconsistency in
global patterns across the genome reinforces the narrative that
mitochondrial and nuclear DNA are distinct entities that are separately
impacted by divergent evolutionary forces, like drift (via population
size) and mutation rates (via kinetic energy). While useful in many
circumstances, mitochondrial DNA should be employed with care, and not
as a broad and convenient proxy for nuclear markers. This distinction is
important because fish mitochondrial genomes are approximately 16 to 17
kb, while nuclear genomes range in size from 300 Mb to 4.5 Gb (Fan et
al. 2020; Satoh et al. 2016), which means that more than 99.99% of the
genome is nuclear. Thus, the nuclear genome contains the majority of
standing genomic variation important for adaptation to changing
conditions and for the speciation process.
Additionally, species-level variation often reduces our power to detect
general macro-scale relationships, and almost certainly contributed to
the lower R2 values reported here. Unsurprisingly, we
found substantial variation in family-specific global gradients of
genetic diversity for 10 families that represented a wide swath of life
history traits. While most of the families followed the general patterns
(at least for mitochondrial diversity) established in the main models,
several instead showed increasing genetic diversity at higher latitudes
and lower SST. Notably, most of these families (including Gadidae and
Sebastidae) are traditionally found in colder, more temperate
environments that also often have higher levels of primary productivity.
If species at these latitudes can support consistently large populations
due to higher resource availability, the relationship with other
important ecological variables, like temperature, might be muted. This
may be the case in our models, as all 10 families displayed either a
positive or quadratic relationship with chlorophyll-a concentration.
Nevertheless, this variation across families is an important reminder
that global patterns are frequently complex, multifaceted, and often the
result of many ecological and species-specific factors.
Generally speaking, macroecological drivers are likely to act in
concert, not isolation, to shape global patterns. Variation in
population size, and subsequently the strength of genetic drift, likely
creates a baseline distribution of genetic diversity, upon which other
evolutionary forces interact to create more complex patterns. Both
mitochondrial and nuclear genetic diversity peaked in communities and
ecosystems with higher resource availability, as represented by primary
productivity. In addition, most models suggested genetic diversity was
elevated closer to the range core, consistent with the central-marginal
hypothesis that suggests population abundance—and subsequently,
genetic diversity—is highest towards the range core where
environmental conditions tend to be optimal (Eckert et al. 2008).
Layered upon these findings, we found evidence that the higher
mitochondrial substitution rates at lower latitudes may serve to
replenish and accumulate diversity at lower latitudes, manifesting in a
traditional latitudinal gradient for mitochondrial diversity that is
highest near the tropics. As nuclear substitution rates are not as
clearly elevated at higher temperatures (Hoffman et al. 2004), similar
latitudinal patterns in nuclear genetic diversity were not apparent.
Life history traits, anthropogenic change, phylogenetic relationships,
and demographic history are also well-known determinants of genetic
diversity, and it is likely these processes influenced our results. For
instance, historically, tropical environments tend to be more stable,
which can enable diversity at both the species and genetic level to
accumulate over time and contribute to the latitudinal diversity
gradients observed here (Rosenzweig 1995).
Range size is also commonly invoked as a driver of latitudinal patterns
of genetic diversity (French et al. 2022; Lawrence & Fraser 2020),
especially when genetic diversity increases towards higher latitudes.
According to Rapoport’s rule, range size grows with latitude (Rapoport
1982), and may be coupled with a rise in genetic diversity because
larger range sizes can support more and larger populations, and even low
levels of gene flow among these demes can increase local genetic
diversity (Waples 2010). However, as access to this range-wide genetic
diversity is mediated by dispersal, there is no guarantee that a
particular population will acquire novel alleles from elsewhere in the
range. While most oceanic taxa likely have high enough rates of gene
flow to facilitate this level of genetic exchange (Palumbi 1992),
studies have found that marine ranges can be much more structured than
previously thought (Pringle & Wares 2011; Selkoe et al. 2016). Future
work explicitly testing the roles of range size and gene flow in
determining general patterns of genetic diversity would help provide
further clarity.
Investigating other DNA markers may also help disentangle the relative
importance of various environmental drivers. In addition to the issues
with mitochondria that we previously discussed, the high mutation rate
of microsatellites, as well as ascertainment bias for highly polymorphic
loci during marker generation, can create extraneous statistical noise
and may be one reason why it was difficult to identify clear spatial
patterns in nuclear diversity. Furthermore, the limited range of
heterozygosity (0-1) can also impose inferential challenges and restrict
the scope of observable patterns. These issues aside, microsatellites
remain one of the most widely available measures of neutral nuclear
genetic diversity and are positively correlated with genome-wide
diversity (Mittel et al. 2015). Moreover, expected heterozygosity is a
robust diversity metric unlikely to be biased by either sampling effort
(Toro et al. 2009) or inbreeding because it is calculated from allele
frequencies (Ritland 1996). While nuclear DNA sequence diversity (e.g.
SNPs, haplotypes) provides a promising next step for future macrogenetic
analyses, standardizing such data across studies remains a substantial
bioinformatic challenge.
Overall, our results reveal disparate global gradients in mitochondrial
and nuclear genetic diversity. While mitochondrial diversity peaks along
the Equator and is positively associated with temperature, mirroring
complementary patterns in marine species, nuclear genetic diversity
shows no strong geographic patterns. Such a lack of clear gradients in
nuclear diversity may be due in part to either evolutionary forces (e.g.
contemporary demographic processes disrupting historical patterns, gene
flow more evenly distributing alleles across species ranges, or
latitudinally consistent mutation rates), analytical ones (e.g. the
reduced statistical power of microsatellites), or a combination of the
two. However, despite these differences, diversity across the genome was
strongly correlated with chlorophyll-a concentrations and was elevated
in regions of higher primary productivity and resource availability that
are able to support larger population densities. Taken together, these
findings enable a better understanding of the degree to which mutation
rates (via elevated temperatures) and drift (via population size) work
collectively to establish large-scale gradients of genetic diversity,
providing a more comprehensive view of how forces interacting across the
genome scale up to provide the starting material for species and
ultimately community diversity.