Introduction
At its core, genetic diversity is the foundation upon which biodiversity
flourishes. It provides the raw material for adaptation to local
environments and divergence among populations. As intraspecific genetic
diversity is the necessary precursor to speciation, exploring global
trends in genetic diversity may shed light on the mechanisms, or
combinations of mechanisms, that drive patterns of species diversity.
Similarly, elucidating the processes that generate genetic diversity
helps create a common ground for evolutionary biology and community
ecology around topics of diversity and patterns of speciation (Vellend
& Geber 2005). Despite this importance, the general patterns of genetic
diversity across species remains poorly understood at global scales (de
Kort et al. 2021; Manel et al. 2020; Messmer et al. 2012; Miraldo et al.
2016). Efforts to understand such trends are vital for identifying the
factors creating and maintaining biodiversity and for pinpointing high
priority areas and taxa for conservation.
Here, we propose three distinct hypotheses for genetic diversity
gradients, all of which are grounded in foundational community ecology
and population genetics theory. The first is the Kinetic Energy
Hypothesis, which posits that, like species richness, intraspecific
genetic diversity should be greater at hotter temperatures due to faster
evolutionary tempos (e.g., higher metabolic and mutation rates),
particularly in mitochondrial DNA that is affected by oxidative damage
from metabolic processes (Allen et al. 2002; Manel et al. 2020; Wright
et al. 2011). While oxidative damage should not influence nuclear DNA
mutation rates (Hoffman et al. 2004), genome-wide mutation rates are
negatively correlated with generation times (Thomas et al. 2010), which
are shorter in organisms with smaller body sizes (Martin & Palumbi
1993), and, by Bergmann’s rule, inversely related to temperature
(Bergmann 1847; Fernández-Torres et al. 2018). Thus, nuclear genetic
diversity may also be weakly correlated with temperature, albeit not to
the degree of mitochondrial diversity (Gillooly et al. 2004). The second
hypothesis, the Productivity-Richness Hypothesis (Evans et al. 2004),
suggests that population size is often constrained by resource
availability, such that regions of high primary productivity should
support larger populations with higher intraspecific genetic variation,
since large populations lose genetic diversity to genetic drift at a
slower rate (Charlesworth 2009; Wright 1983). Finally, the Founder
Effect Hypothesis proposes a negative relationship between latitude and
genetic diversity, a lasting legacy from the last glacial maximum (LGM)
(Hewitt 2000). As species expanded from equatorial to temperate and
polar latitudes, a sequential series of founder and bottleneck events
along the expansion front depleted standing genetic variation, leaving a
latitudinal genetic footprint that is still apparent in many modern
populations (Jenkins et al. 2018; Lessa et al. 2010; Mattingsdal et al.
2020). For marine species, this effect is particularly pronounced in the
Northern hemisphere, as many contemporary high-latitude taxa in the
Southern Ocean may have endured the LGM in local polar refugia (Allcock
& Strugnell 2012; Fraser et al. 2012).
Much of our knowledge on intraspecific genetic diversity, including
local and regional estimates in various taxa, has only been collected in
recent decades. Recent studies compiled these data to construct
broad-scale geographic patterns in order to better understand global
distributions of genetic diversity (Li et al. 2021; Manel et al. 2020;
Miraldo et al. 2016). For example, Martin & McKay (2004) revealed
greater genetic divergence among vertebrate populations at lower
latitudes, while Schmidt et al. (2022) found that environmental
heterogeneity was an important predictor of genetic diversity in North
American mammals. Large knowledge gaps still exist, however, as the
strength and direction of latitudinal gradients in genetic diversity
appear to vary across taxa and ecological systems (de Kort et al. 2021).
In particular, it remains unclear how universal such patterns are and
how influential underlying ecological drivers may be. This is
particularly true of marine communities, as most meta-analyses of global
genetic diversity to date have focused on either terrestrial or
freshwater systems (but see Manel et al. 2020).
While the same evolutionary processes occur in all taxa, the strength of
these forces (particularly selection, drift, and gene flow) differ
substantially across terrestrial and marine realms (Steele et al. 2019;
Strathmann 1990). Marine species tend to exhibit larger populations,
higher gene flow, and wider species ranges (Steele et al. 2019). Alleles
may be more easily transported throughout species ranges and latitudes
in marine systems, muting the effects of the local environment and
weakening the consequences of genetic drift. Such patterns have
previously been documented, including evidence that strong dispersal
helped maintain high diversity in range edge populations of Senegal
seabream, Diplodus bellottii , and erased typical core-periphery
patterns of genetic variation (Robalo et al. 2020). Moreover, global
patterns of species richness tend to differ between land and sea. Marine
taxa commonly display bimodal latitudinal gradients of species richness
(Chaudhary 2016; Tittensor et al. 2010), peaking at mid-latitudes
instead of along the equator as is more common in their terrestrial
counterparts (Davies et al 2007; Rolland et al 2014). Given these unique
differences, more work is needed to determine how the distinctive
environmental conditions and life-history strategies in the ocean
combine to shape macroecological patterns of genetic diversity.
In addition, most macrogenetic studies have primarily investigated
patterns of mitochondrial genetic diversity, despite suggestions that
such markers do not accurately reflect nuclear genetic diversity (Bazin
et al. 2006; Leigh et al. 2021). For example, putatively neutral
mitochondrial markers are linked without recombination to loci under
strong selective constraints (Galtier et al. 2009). Mitochondrial
diversity is therefore subject to selective sweeps and background
selection as well as bottlenecks due to its small effective population
size (Ne ), which is a quarter that of nuclear DNA
(Ballard & Whitlock 2003; Birky et al. 1989). Mitochondrial diversity
does not display a consistent relationship with population size, with
strong variation across taxa that is not related to population size or
life history characteristics (Bazin et al. 2006; James & Eyre-Walker
2020; Nabholz et al. 2009). The Resource Availability Hypothesis,
therefore, may apply most strongly to nuclear diversity, and only weakly
to mitochondrial diversity. However, the Founder Effect Hypothesis may
apply more strongly to mitochondrial genetic diversity, as mitochondrial
DNA should be more sensitive to bottleneck events and founder effects
from the LGM due to its smaller Ne (Birky et al.
1989). With these caveats in mind, macro-scale patterns of mitochondrial
genetic variation may not be generalizable across the genome. To gain a
more complete understanding of global distributions of genetic
diversity, neutral genetic variation should also be analyzed across the
nuclear genome to understand forces acting across this much larger
fraction of the genome.
To help close these knowledge gaps, we conducted a literature search to
aggregate georeferenced data from population genetic studies in marine
fish species and then used these data to evaluate the three hypotheses.
We compiled environmental data on sea surface temperature (SST) and
chlorophyll (a proxy for primary productivity) and assessed the
generality of these hypotheses using both mitochondrial and nuclear
(microsatellite) DNA. Specifically, we tested 1) the Kinetic Energy
Hypothesis that temperature and genetic diversity will be positively
related most strongly in mitochondrial DNA and more weakly in nuclear
DNA, 2) the Resource Availability Hypothesis that primary productivity
(e.g., chlorophyll) will be positively related with genetic diversity,
particularly in nuclear DNA, and 3) the Founder Effect Hypothesis that
both mitochondrial and nuclear genetic diversity will be negatively
correlated with latitude and increase towards the equator, particularly
in the Northern hemisphere and more strongly in mitochondrial diversity.
To test among these three hypotheses, we fit generalized linear mixed
effect models (GLMMs) and explored the extent to which each
macroecological driver independently explained variation in
mitochondrial or nuclear genetic diversity.