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 new species, 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. We found that mitochondrial genetic diversity was
highest at lower latitudes and in the Coral Triangle, consistent with
similar patterns of marine taxonomic diversity. However, these patterns
were not replicated for nuclear diversity, which showed neither strong
latitudinal nor longitudinal patterns. Compounding these genome-wide
differences, we also found a significant, positive relationship between
temperature and mitochondrial genetic diversity, but not for nuclear
diversity. In contrast, both mitochondrial and nuclear diversity were
related to chlorophyll concentrations. Overall, these results suggest
that nuclear and mitochondrial genetic diversity are generated and
maintained by different, albeit overlapping, macroecological processes
that scale up to produce distinct global diversity gradients.
Previous studies have found latitudinal gradients in mitochondrial
genetic diversity, mirroring our results here (Manel et al. 2020;
Miraldo et al. 2016). However, the methods and statistical analyses
frequently employed by these studies have come under recent criticism
(Gratton et al. 2017, Paz-Vinas et al. 2021). Most earlier macrogenetic
studies pooled samples and sequences into predefined grid cells or
latitudinal bands, calculated diversity at the species level, and then
averaged 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, or for the relative frequency of
individual haplotypes within each population (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). After accounting for issues of within-species geographic
variation and relative haplotype abundance, our research here showed
that mitochondrial diversity still had clear latitudinal and
longitudinal patterns, peaking at lower latitudes and in the
Indo-Pacific. Given the similarity with species diversity patterns in
the ocean (Manel et al. 2020; Tittensor et al. 2010), these results may
provide an important mechanistic link between processes generating
genetic diversity within the population and those that drive diversity
patterns at higher levels of biological organization.
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 & Fraser 2021), and plants (de Kort et
al. 2021). 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. Species-level variation may further reduce any
power to detect general macro-scale relationships. When compared to the
clear 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. 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 mean 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 or the speciation process.
Overall, we found that nuclear genetic diversity was most strongly
correlated with chlorophyll, a proxy for primary productivity and
resource availability, while mitochondrial diversity was tightly
associated with chlorophyll, sea surface temperature, latitude, and
longitude. Taken together, these results provide support for each of the
three hypotheses to varying degrees. The positive relationship between
chlorophyll and genetic diversity across the genome provides strong
evidence for the Productivity-Richness Hypothesis and suggests that
regions of higher productivity facilitate larger population sizes, and
in turn, higher levels of genetic variation. 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 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 previously 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 not far from 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).
Each of these proposed 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 most 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.
Taken together, global patterns in mitochondrial genetic diversity
appear to be influenced by mutation rates, drift, andNe , while nuclear diversity is determined
primarily by drift and population size.
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.
While we accounted for some of these processes in our models, there are
almost certainly other factors left unaccounted for that likely
contributed to the patterns we observed. In particular, range size is
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 increases with latitude (Rapoport 1982), and
is often 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 these and additional 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 in particular 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 clear yet 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 is strongly correlated with chlorophyll and is
elevated in regions of high 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.