Global determinants of freshwater and marine fish genetic diversity

Abstract

Genetic diversity is estimated to be declining faster than species diversity under escalating threats, but its spatial distribution remains poorly documented at the global scale. Theory predicts that similar processes should foster congruent spatial patterns of genetic and species diversity, but empirical studies are scarce. Using a mined database of 50,588 georeferenced mitochondrial DNA barcode sequences (COI) for 3,815 marine and 1,611 freshwater fish species respectively, we examined the correlation between genetic diversity and species diversity and their global distributions in relation to climate and geography. Genetic diversity showed a clear spatial organisation, but a weak association with species diversity for both marine and freshwater species. We found a predominantly positive relationship between genetic diversity and sea surface temperature for marine species. Genetic diversity of freshwater species varied primarily across the regional basins and was negatively correlated with average river slope. The detection of genetic diversity patterns suggests that conservation measures should consider mismatching spatial signals across multiple facets of biodiversity.

Fig. 1. Biogeographic patterns of fish genetic diversity.

Genetic diversity was estimated as the mean number of mutations per base pair for Cytochrome Oxidase Subunit 1 sequence across species (a) 514 cells for marine fishes and (c) 343 cells for freshwater fishes. The colour gradient represents the relative variation of intraspecific genetic diversity: the reddest square cells have the highest genetic diversity. The colour scale of Fig. 1a, c is defined in the Fig. 1c: the bluest square cells have the lowest genetic diversity. Genetic diversity was averaged across cells within latitudinal band of 10° and is plotted as a function of latitude for marine species (b) and freshwater species (d) with error bars representing confidence intervals (standard deviation of mean genetic diversity across cells/square root of the number of cells) and indicates variability of genetic diversity among cells. The grey colour gradient indicates the number of cells used in each latitudinal band. The grey colour scale is defined in Fig. 1d. For the fish silhouette in Fig. 1d, credit given to U.S. Fish and Wildlife Service (illustration) and T. J. Bartley with licence at: http://www.phylopic.org/image/f8369dec-bdf6-432b-a0c4-41ee5d75286d/. Drawn with R version 3.2.3.

Fig. 2. Congruence between fish genetic and species diversity.

Classification of cells depending simultaneously of their values of genetic and species diversity for marine (a) and freshwater (c) species. Values of diversity were reported on the global map using a colour gradient depending on the values of the genetic and species diversities for marine species (b) and freshwater species (d) respectively. The colour scale of Fig. 2a–d is defined in the Fig. 2d. The line was represented as the output of a linear model (lm) of the correlation between genetic diversity and species diversity. Person coefficient of correlations calculated in linear regressions (r) are reported on the figure. Drawn with R version 3.2.3.

Fig. 3. Determinants of fish genetic diversity patterns.

Outputs of the linear models (lm) testing the effect of geographic, environmental and sampling factors on the global pattern of marine (a, b) and freshwater (c, d) genetic diversity (See Supplementary Table 3 and 5 for details on models). Coefficients and confidence intervals for the factors of the models for marine (a) and freshwater fishes (c). Confidence intervals were estimated from the standard error of each coefficient at a level of 5% and were obtained with the command confint in the R package lm. Autocor is a spatial autocovariate that takes into account spatial autocorrelation in both our predicted and predictive variables. Relative variance of genetic diversity explained by the various factors was estimated and represented as partial plots with the package hier.part in marine (b) and in freshwater fishes (e).