Reconstruction of body mass evolution in the Cetartiodactyla and mammals using phylogenomic data

Abstract

Reconstructing ancestral characters on a phylogeny is an arduous task because the observed states at the tips of the tree correspond to a single realization of the underlying evolutionary process.Recently, it was proposed that ancestral traits can be indirectly estimated with the help of molecular 30 data, based on the fact that life history traits influence substitution rates. Here we challenge these new approaches in the Cetartiodactyla, a clade of large mammals which, according to paleontology, derive from small ancestors. Analysing transcriptome data in 41 species, of which 22 were newly sequenced, we provide a dated phylogeny of the Cetartiodactyla and report a significant effect of body mass on the overall substitution rate, the synonymous vs. non-synonymous substitution rate 35 and the dynamics of GC-content. Our molecular comparative analysis points toward relatively small Cetartiodactyla ancestors, in agreement with the fossil record, even though our data set almost exclusively consists of large species. This analysis demonstrates the potential of phylogenomic methods for ancestral trait reconstruction and gives credit to recent suggestions that the ancestor to placental mammals was a relatively large and long-lived animal. 40

Inferring long-term effective population size with Mutation-Selection models

“…This is consistent with the expectation that small-sized and short-lived species tend to be characterized by larger effective population sizes (Romiguier et al, 2014). Of note, these results mirror previous findings, based on classical codon models, showing that d N /d S tends to be positively correlated with LHTs (Lartillot and Delsuc, 2012;Nabholz et al, 2013;Figuet et al, 2017). Result which was also recovered on the present dataset, using a Thus, altogether, the inferred trends in N e across species appear to be as expected, based on considerations about life-history evolution.…”

“…Analyses using these approaches and these proxies of N e have suggested a negative correlation between (Popadin et al, 2007;Lanfear et al, 2010;Lartillot and Poujol, 2011;Lartillot and Delsuc, 2012;Romiguier et al, 2014;Figuet et al, 2017), thus confirming the theoretical prediction of the nearlyneutral theory. However, the universality and robustness of the correlation between d N /d S and N e is still debated (Nabholz et al, 2013;Lanfear et al, 2014;Figuet et al, 2016;Bolívar et al, 2019), and further investigation might be required.…”

“…The reconstructions obtained on several empirical datasets, in particular in mammals and in isopods, suggest that the method is able to correctly infer the directional trends of the changes in N e across species. In particular, in mammals, the inferred variation in N e correlates negatively with body size and, more generally, Figuet et al (2017). Similarly, in isopods, smaller effective population sizes are inferred in subterranean species, again, as expected (Capderrey et al, 2013).…”

Predicting small ancestors using contemporary genomes of large mammals

“…One intriguing application of this idea is to exploit the apparent correlation between substitution rates and body size to infer ancestral species' body sizes using the inferred patterns of substitution rate variation among species lineages based on genomes of extant species [1]. The recommended paper by Figuet et al [2] examines the utility of such approaches by analyzing the Cetartiodactyla, a clade of large mammals that have mostly well resolved phylogenetic relationships and a reasonably good fossil record. This combination of genomic data and fossils allows a direct comparison between body size predictions obtained from the genomic data and empirical evidence from the fossil record.…”

“…If predictions seem good in groups such as the Cetartiodactyla, where there is independent evidence from the fossil record, this would increase the credibility of predictions made for species with less abundant fossils. Figuet et al [2] analyze transcriptome data for 41 species and report a significant effect of body mass on overall substitution rate, synonymous vs. nonsynonymous rates, and the dynamics of GC-content, thus allowing a prediction of small ancestral body size in this group despite the fact that the extant species that were analyzed are nearly all large. A comparative method based solely on morphology and phylogenetic relationships would be very unlikely to make such a prediction.…”