Mitochondrial genomes reveal slow rates of molecular evolution and the timing of speciation in beavers (Castor), one of the largest rodent species

Abstract

Background: Beavers are one of the largest and ecologically most distinct rodent species. Little is known about their evolution and even their closest phylogenetic relatives have not yet been identified with certainty. Similarly, little is known about the timing of divergence events within the genus Castor.

Methodology/principal findings: We sequenced complete mitochondrial genomes from both extant beaver species and used these sequences to place beavers in the phylogenetic tree of rodents and date their divergence from other rodents as well as the divergence events within the genus Castor. Our analyses support the phylogenetic position of beavers as a sister lineage to the scaly tailed squirrel Anomalurus within the mouse related clade. Molecular dating places the divergence time of the lineages leading to beavers and Anomalurus as early as around 54 million years ago (mya). The living beaver species, Castor canadensis from North America and Castor fiber from Eurasia, although similar in appearance, appear to have diverged from a common ancestor more than seven mya. This result is consistent with the hypothesis that a migration of Castor from Eurasia to North America as early as 7.5 mya could have initiated their speciation. We date the common ancestor of the extant Eurasian beaver relict populations to around 210,000 years ago, much earlier than previously thought. Finally, the substitution rate of Castor mitochondrial DNA is considerably lower than that of other rodents. We found evidence that this is correlated with the longer life span of beavers compared to other rodents.

Conclusions/significance: A phylogenetic analysis of mitochondrial genome sequences suggests a sister-group relationship between Castor and Anomalurus, and allows molecular dating of species divergence in congruence with paleontological data. The implementation of a relaxed molecular clock enabled us to estimate mitochondrial substitution rates and to evaluate the effect of life history traits on it.

Figure 1. Distribution of beavers and sampling sites.

Beavers live in North America (C. canadensis, striped areas) and Eurasia (C. fiber, grey areas). Black areas mark C. fiber relict populations from which the current populations developed. C. canadensis was introduced in Europe and Asia (striped areas, distribution not exactly known for Kamchatka). Numbers indicate beaver populations sampled for mitochondrial genome sequencing. C. fiber was sampled in the areas of the relict populations (1,3,4,5) or close to them (2) . C. canadensis was sampled in a European introduced population (6). Arrow: migration via the Bering land bridge is suggested to have initiated Castor speciation around 8–7.6 million years ago (mya). Map redrawn from , and .

Figure 2. Sequencing coverage plots of beaver mitochondrial genomes.

Plots for C.f. ssp. birulai amplified by long range PCR (grey line) and C.f. ssp. pohlei enriched by hybridization capture (black line). Coverage was more even when hybridization capture was used instead of long range PCR. Peaks of sequencing coverage are visible for C.f. ssp. birulai (grey) in proximity to priming sites (indicated on top of the plots).

Figure 3. Timetree of rodents and outgroups.

Beavers share a common ancestor with Anomaluromorpha around 54 mya (CI: 44–64 mya); the only extant beaver genus Castor separated into two species from 8–7.6 mya onwards (CI: 3.7–13 mya). The common ancestor of the Eurasian relict populations was estimated to have lived around 210,000 ya (CI: 0.11–0.34 mya). The tree depicted is a maximum clade credibility tree from BEAST analyses based on a 16,352 bp alignment (including gaps). Bayesian posterior probability (>0.6) and bootstrap support values (>50) are shown at the branches and separated by slashes for MrBayes, maximum likelihood, neighbor joining and maximum parsimony, respectively. Diamonds indicate fossil calibrations (Table S4). Paleoc.: Paleocene; Oligoc.: Oligocene; Pl: Pliocene, PH: Pleistocene and Holocene. Castor fiber po, tu, bi, in and al indicate the subspecies sampled (see Table S1).

Figure 4. Comparison of mitochondrial substitution rates among glires.

Phylogenetic tree of glires (rodents and lagomorphs) with branch lengths from the BEAST analysis. Mitochondrial substitution rates are shown on the branches or next to each taxon in units of substitutions per million years. Beavers exhibit short branches and substitution rates for beavers are the lowest within the mouse-related clade, significantly lower than those of most other rodents (see also Table 1).

Figure 5. Linear regression of average substitution rates and lifespan of rodents.

Rodents with higher mitochondrial substitution rates exhibit a shorter lifespan (R squared  = 0.4011, p-value  = 0.0113). See Table S6 and S7 for details.