The time-dependent evolutionary rate of mitochondrial DNA in small mammals inferred from biogeographic calibration points with reference to the late Quaternary environmental changes in the Japanese archipelago

Abstract

Mitochondrial DNA (mtDNA) sequences have long been the most popular marker for assessing phylogenetic relationships and uncovering population dynamics. However, the mechanism of the nucleotide substitution rate of mtDNA remains unclear. While the evolutionary rate over tens of thousands of years is thought to be time dependent, the overall picture is not fully understood. This article presents recent achievements related to the time-dependent evolutionary rate of mtDNA in small rodents in the Japanese archipelago. The method focuses on rapid expansion events during the late Quaternary, during which there was a prolonged severe cold period and repeated abrupt warm periods, providing multiple calibration points. The global sea level fluctuation and migration to islands help to specify the calibration points. For calibration points at 11000, 15000, 53000, and 130000 years ago, the evolutionary rates were approximately 0.11, 0.11, 0.047, and 0.029 substitutions/site/million years, respectively, in the mitochondrial cytochrome b gene (Cytb). Applying the higher rate to assess the evolutionary history of the commensal house mouse (Mus musculus) and complete mitochondrial genome sequences (~16000 bp) allowed us to trace prehistoric human culture development based on millet and rice agriculture. The pattern of time-dependent evolutionary rates presented here is likely applicable to other small rodents. The Japanese archipelago is ideal for assessing evolutionary rates with biogeographic calibration points in the late Quaternary in species with multiple genetically distinct local populations.

Temporal dynamics of mildly deleterious nonsynonymous substitutions in mitochondrial gene sequences in rodents and moles

“…S2) with Arlequin v3.5.1.2 (Excoffier and Lischer, 2010), providing modes of pairwise nucleotide differences (τ values). We categorized the 23 haplogroups into three groups for convenience, according to expansion start times: post-LGM (Group I), early MIS 3 (Group II) and post-PGM (Group III) (Suzuki et al, 2015;Hanazaki et al, 2017;Honda et al, 2019;Nakamoto et al, 2021;Suzuki, 2021), in which the range of the τ values for each group was as follows: Group I, τ < 4.1; Group II, 5 < τ < 6.3; and Group III, τ > 7.2. Haplogroup m of A. sylvaticus from Sicily, which had an estimated expansion start time of 230,000 years ago (Suzuki, 2021), was integrated into Group III.…”

“…As nonsynonymous substitutions are the best candidates for substitutions that can be categorized as mildly deleterious in mtDNA protein-coding sequences, we focused on the dynamics of nonsynonymous substitutions by measuring pN using 23 haplogroups exhibiting a genetic signature of rapid expansion. We categorized the haplogroups into Groups I, II and III, which correspond to the post-LGM (the last 15,000 years), early MIS 3 (53,000 years ago) and post-PGM (130,000 years ago) time frames, respectively (Suzuki, 2021). The overall networks, especially those of the haplogroups in Groups II and III, were star-shaped, Estimates of the time elapsed since expansion, with the previously predicted evolutionary rates of 0.11, 0.047 and 0.028 substitutions/site/million years for Groups I, II and III, respectively (Honda et al, 2019;Suzuki, 2021).…”

“…We categorized the haplogroups into Groups I, II and III, which correspond to the post-LGM (the last 15,000 years), early MIS 3 (53,000 years ago) and post-PGM (130,000 years ago) time frames, respectively (Suzuki, 2021). The overall networks, especially those of the haplogroups in Groups II and III, were star-shaped, Estimates of the time elapsed since expansion, with the previously predicted evolutionary rates of 0.11, 0.047 and 0.028 substitutions/site/million years for Groups I, II and III, respectively (Honda et al, 2019;Suzuki, 2021). 1 for details) represent three rodent groups: the house mouse Mus musculus (A, B, F), voles of the genera Myodes (E, G, H, I) and Microtus (K), and wood mice of the genus Apodemus (C, D, J, L, M).…”

“…In these plots we used τ values normalized to a length of 1140 bp in haplogroups f, j and m. Assignment of nonsynonymous and synonymous substitutions responsible for the time-dependent evolutionary rates of rodent mtDNA observed in Groups I, II and III (C). The time-dependent evolutionary rates have been assessed in previous studies: 0.11, 0.047 and 0.028 substitutions/site/myr for Groups I, II and III, respectively (Honda et al, 2019;Suzuki, 2021). Setting possible representative values of pN, partitioned evolutionary rates of non synonymous (Nμ) and synonymous (Sμ) substitutions were calculated for each group of haplogroups (see text for details).…”

“…These in turn allow us to calculate evolutionary rates, based on the modal (peak) values of a unimodal mismatch distribution, defined as τ, which is a statistical value proportional to the time since expansion. The resulting evolutionary rate is 0.11 substitutions/site/million years (myr) for divergence within the past 10,000 years, followed by a sharp decrease to approximately 0.03 substitutions/site/myr for divergence that occurred more than 130,000 years ago (Suzuki et al, 2015;Hanazaki et al, 2017;Honda et al, 2019;Suzuki, 2021). To trace the dynamics of nonsynonymous substitutions, it is also reasonable to address those lying on the younger and older branches of the haplogroup network.…”