Past climate-driven range shifts structuring intraspecific biodiversity levels of the giant kelp (Macrocystis pyrifera) at global scales

Abstract

The paradigm of past climate-driven range shifts structuring the distribution of marine intraspecific biodiversity lacks replication in biological models exposed to comparable limiting conditions in independent regions. This may lead to confounding effects unlinked to climate drivers. We aim to fill in this gap by asking whether the global distribution of intraspecific biodiversity of giant kelp (Macrocystis pyrifera) is explained by past climate changes occurring across the two hemispheres. We compared the species' population genetic diversity and structure inferred with microsatellite markers, with range shifts and long-term refugial regions predicted with species distribution modelling (SDM) from the last glacial maximum (LGM) to the present. The broad antitropical distribution of Macrocystis pyrifera is composed by six significantly differentiated genetic groups, for which current genetic diversity levels match the expectations of past climate changes. Range shifts from the LGM to the present structured low latitude refugial regions where genetic relics with higher and unique diversity were found (particularly in the Channel Islands of California and in Peru), while post-glacial expansions following ~ 40% range contraction explained extensive regions with homogenous reduced diversity. The estimated effect of past climate-driven range shifts was comparable between hemispheres, largely demonstrating that the distribution of intraspecific marine biodiversity can be structured by comparable evolutionary forces across the global ocean. Additionally, the differentiation and endemicity of regional genetic groups, confers high conservation value to these localized intraspecific biodiversity hotspots of giant kelp forests.

Figure 1

Potential distribution of Macrocystis pyrifera estimated with Species Distribution Modelling for (panels A and B) the present and (panels C and D) the last glacial maximum (yellow and red colors depicting surface and subtidal habitats down to 30 m depth, respectively). Sea ice extent is depicted in white. Detailed maps per continent available in Figs. 6–9 in S3. Occurrence records used in Species Distribution Modelling in Fig. 10 in S3.

Figure 2

Genetic structure of Macrocystis pyrifera. (panel A) Network analysis based on shared allele distance. Red circles in the network identify sites with higher network centrality (> 95th percentile of centrality). (panel B) Structure analysis for the first and second hierarchical levels of subdivision with bars representing the proportion of individual assignments to each cluster. Analyses using the DeltaK criterion to infer the number of K clusters available in S3: first hierarchical level with K = 2 or 4; second hierarchical level with K = 4 and K = 2. Colors depict distinct genetic groups and the numbers label populations of interest. (panel C) Second hierarchical level of genetic subdivision (proportion of individual assignments to each cluster). Sea ice extent is depicted in white.

Figure 3

Standardized genetic diversity per site as a function of (panels A and B) distance to closest glacial refugia (version considering the natural logarithm of distance in Fig. 4 in S3). Colors depicting the assignment of populations to the different genetic clusters (as in Fig. 2). Standardized diversity per genetic group for the (panel C) first and (panel D) second hierarchical levels of genetic subdivision. Population pairwise differentiation (Jost's D, average) between genetic groups inferred for the (panel C) first and (panel D) second levels of genetic subdivision. Asterisks depict groups with significantly higher genetic diversity.