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.