Introduction
At its core, genetic diversity is the foundation upon which biodiversity
flourishes. Intraspecific genetic diversity can help drive speciation
events by enabling adaptation to novel environments and reduce
extinction risk by providing a genomic reservoir during periods of
environmental change (Vellend & Geber, 2005). Exploring global trends
in genetic diversity can shed light on the mechanisms, or combinations
of mechanisms, that drive 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 remain 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.
Much of our knowledge on intraspecific genetic diversity, including
local and regional estimates in various taxa, has only been collected in
recent decades. Recent macrogenetic studies have compiled these data to
construct broad-scale geographic patterns and 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 macrogenetic studies 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 within individual species, 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). Marine species also have strong longitudinal patterns in species
diversity, with greatest species biodiversity in the Indo-Pacific Coral
Triangle due in part to higher habitat availability and sea surface
temperatures (Sanciangco et al. 2013). Given these differences, it
remains unclear how environmental conditions and life history strategies
in the ocean combine to shape macroecological patterns of genetic
diversity. Recent studies have begun to investigate these questions,
including Manel et al. (2020)’s finding that mitochondrial genetic
diversity in marine fishes was positively correlated with sea surface
temperature. However, the mitochondrial genome is a small (less than
0.01%) fraction of the genetic material in fish, and more work is
needed to understand the ubiquity of these observed patterns across the
genome.
Most macrogenetic studies have investigated patterns of mitochondrial
genetic diversity, despite suggestions that such markers do not
accurately reflect neutral nuclear genetic diversity (Bazin et al. 2006;
Leigh et al. 2021). For example, many 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 also does not display a consistent
relationship with population size, with strong variation across taxa
that is not related to life history characteristics (Bazin et al. 2006;
James & Eyre-Walker 2020; Nabholz et al. 2009). With these caveats in
mind, macro-scale patterns of mitochondrial genetic variation may not be
generalizable to nuclear diversity. To gain a more complete
understanding of global distributions of genetic diversity, neutral
genetic variation in the much larger nuclear genome should also be
analyzed.
Here, we propose three distinct hypotheses for global 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-Diversity 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 greater intraspecific genetic variation,
since large populations lose genetic diversity to genetic drift at a
slower rate (Charlesworth 2009; Wright 1983). However, this relationship
may reverse in regions with particularly high levels of productivity -
as more individuals and species are supported, resources become
increasingly divided, causing population sizes and subsequently, genetic
diversity, to decline (Lawrence & Fraser, 2020). 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 may have depleted standing genetic variation
and left 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 could be particularly
pronounced in the Northern hemisphere, as many contemporary
high-latitude taxa in the Southern Ocean endured the LGM in local polar
refugia (Allcock & Strugnell 2012; Fraser et al. 2012). The Founder
Effect Hypothesis may also apply more strongly to mitochondrial
diversity, as mitochondrial DNA should be more sensitive to bottleneck
events and founder effects from the LGM due to its smallerNe (Birky et al. 1989).
To help better identify and understand global patterns in marine genetic
diversity, we conducted a literature search to aggregate georeferenced
data from population genetic studies in marine fish species and then
used these data to evaluate these three hypotheses. We compiled
environmental data on sea surface temperature (SST) and chlorophyll-a
concentration (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 Productivity-Diversity Hypothesis that genetic diversity
will be highest in regions with mid-to-high levels of primary
productivity (e.g. chlorophyll-a), particularly in nuclear DNA (as it is
more closely related to population size, the mediating factor), 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 explained
variation in mitochondrial or nuclear genetic diversity.