Meta-analysis of northeast Atlantic marine taxa shows contrasting phylogeographic patterns following post-LGM expansions

Abstract

Background: Comparative phylogeography enables the study of historical and evolutionary processes that have contributed to shaping patterns of contemporary genetic diversity across co-distributed species. In this study, we explored genetic structure and historical demography in a range of coastal marine species across the northeast Atlantic to assess whether there are commonalities in phylogeographic patterns across taxa and to evaluate whether the timings of population expansions were linked to the Last Glacial Maximum (LGM).

Methods: A literature search was conducted using Web of Science. Search terms were chosen to maximise the inclusion of articles reporting on population structure and phylogeography from the northeast Atlantic; titles and abstracts were screened to identify suitable articles within the scope of this study. Given the proven utility of mtDNA in comparative phylogeography and the availability of these data in the public domain, a meta-analysis was conducted using published mtDNA gene sequences. A standardised methodology was implemented to ensure that the genealogy and demographic history of all mtDNA datasets were reanalysed in a consistent and directly comparable manner.

Results: Mitochondrial DNA datasets were built for 21 species. The meta-analysis revealed significant population differentiation in 16 species and four main types of haplotype network were found, with haplotypes in some species unique to specific geographical locations. A signal of rapid expansion was detected in 16 species, whereas five species showed evidence of a stable population size. Corrected mutation rates indicated that the majority of expansions were estimated to have occurred after the earliest estimate for the LGM (∼26.5 Kyr), while few expansions were estimated to have pre-dated the LGM.

Conclusion: This study suggests that post-LGM expansion appeared to be common in a range of marine taxa, supporting the concept of rapid expansions after the LGM as the ice sheets started to retreat. However, despite the commonality of expansion patterns in many of these taxa, phylogeographic patterns appear to differ in the species included in this study. This suggests that species-specific evolutionary processes, as well as historical events, have likely influenced the distribution of genetic diversity of marine taxa in the northeast Atlantic.

Keywords: Comparative phylogeography; Historical demography; Last Glacial Maximum; Northeast Atlantic; Population expansion; mtDNA.

Figure 1. Topographical map of the northeast Atlantic Ocean.

The white dotted lines represent the maximum extent of ice cover during the Last Glacial Maximum (LGM) (redrawn from Hughes et al., 2016). Orange lines indicate putative refugia: Hurd Deep, Brittany and Iberia.

Figure 2. Haplotype networks showing four different network structures.

Haplotype networks showing (A) ‘star’ (Palinurus elephas), (B) ‘complex star’ (Carcinus maenas), (C) ‘reciprocally monophyletic’ (Macoma balthica) and (D) ‘complex mutational’ (Dicentrarchus labrax) structures. Each circle represents a unique haplotype and the sizes of the circles are proportional to the haplotype frequencies for each network but are not comparable across studies. Each line represents one mutation step and two or more steps are indicated by bars or numbers. Colours inside the circles correspond to sites which have individuals represented in that particular haplotype. Species illustrations by Guy Freeman.

Figure 3. Mismatch distributions showing four different distributions.

Mismatch distributions showing (A) unimodal (Maja brachydactyla), (B) skewed unimodal (Nassarius reticulatus), (C) multimodal (Labrus bergylta) and (D) bimodal (Macoma balthica). Unimodal and skewed unimodal distributions are generally associated with a sudden expansion and a recent sudden expansion, respectively. Multimodal and bimodal are thought to be associated with a constant population size (but see text). Bars represent the frequency of pairwise nucleotide differences between individuals. Curves correspond to the expected distribution fitted to the data under a model of constant population size (solid line) or demographic expansion (dotted line). Species illustrations by Guy Freeman.

Figure 4. Estimated dates of expansion for species or lineages (L) in which the demographic expansion hypothesis was not rejected.

A minimum and maximum time since expansion is plotted as horizontal bars for some datasets, estimated from a minimum and maximum mutation rate (Table S1). The beginning of the last glacial period (dotted line) and the estimated time-frame of the Last Glacial Maximum (grey shaded area) are displayed. Species are organised by taxa: crustaceans, Carcinus maenas –Palinurus elephas); fish, Conger conger –Symphodus melops; macroalgae, Pelvetia canaliculata; molluscs, Cerastoderma edule –Nassarius reticulatus; polychaetes, Owenia fusiformis –Pectinaria koreni. Species illustrations by Guy Freeman.

Figure 5. Bayesian Skyline Plots for species or lineages (L) in which the demographic expansion hypothesis was not rejected.

Solid black lines show the medium effective population size over time (N_e = effective population size and T = generation time); dashed black lines represent the 95% confidence intervals. The estimated time-frame of the Last Glacial Maximum is denoted by the area shaded dark grey. Species are organised by taxa: crustaceans, Carcinus maenas (A), Maja brachydactyla (B), Palinurus elephas (C); fish, Conger conger (D), Dicentrarchus labrax (E), Labrus bergylta (F), Pomatoschistus microps (G), P. minutus (H), Solea solea (I), Symphodus melops (J); macroalgae, Pelvetia canaliculata (K); molluscs, Cerastoderma edule (L), Modiolus modiolus Lineage 1 (M), Nassarius reticulatus (N); polychaetes, Owenia fusiformis Lineage 1 (O), O. fusiformis Lineage 2 (P), O. fusiformis Lineage 3 (Q), Pectinaria koreni Lineage 1 (R), P. koreni Lineage 2 (S).