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.