Towards understanding paleoclimate impacts on primate de novo genes

Abstract

De novo genes are genes that emerge as new genes in some species, such as primate de novo genes that emerge in certain primate species. Over the past decade, a great deal of research has been conducted regarding their emergence, origins, functions, and various attributes in different species, some of which have involved estimating the ages of de novo genes. However, limited by the number of species available for whole-genome sequencing, relatively few studies have focused specifically on the emergence time of primate de novo genes. Among those, even fewer investigate the association between primate gene emergence with environmental factors, such as paleoclimate (ancient climate) conditions. This study investigates the relationship between paleoclimate and human gene emergence at primate species divergence. Based on 32 available primate genome sequences, this study has revealed possible associations between temperature changes and the emergence of de novo primate genes. Overall, findings in this study are that de novo genes tended to emerge in the recent 13 MY when the temperature continues cooling, which is consistent with past findings. Furthermore, in the context of an overall trend of cooling temperature, new primate genes were more likely to emerge during local warming periods, where the warm temperature more closely resembled the environmental condition that preceded the cooling trend. Results also indicate that both primate de novo genes and human cancer-associated genes have later origins in comparison to random human genes. Future studies can be in-depth on understanding human de novo gene emergence from an environmental perspective as well as understanding species divergence from a gene emergence perspective.

Keywords: de novo genes; gene emergence; gene evolution; paleoclimate; primate genes.

Fig. 1.

A timetree of 32 primate species. The node and branch of Cebus imitator was obtained from Boubli et al. (2012) and integrated into the timetree. Divergence times of the other 31 species were obtained from the TimeTree database (Kumar et al. 2022). The confidence interval for divergence times on TimeTree is 95%, indicating that approximately 95% of reported times in the synthesized studies lie within 2 SDs of the mean time, assuming a normal distribution.

Fig. 2.

Estimated number of emerged human genes overlayed on temperature change associated with time. Blue markers represent primate or human de novo genes obtained from Evans et al. (2006); Li et al. (2010); Wu et al. (2011); Xie et al. (2012); Suenaga et al. (2014); Wang et al. (2014); Chen et al. (2015); Ruiz-Orera et al. (2015); Zhang et al. (2015); McLysaght and Hurst (2016); Kalebic et al. (2018); Suzuki et al. (2018); Sun et al. (2020); Yang et al. (2020); Saber et al. (2021), red markers starting at 13 on the y-axis represent cancer-associated genes, orange markers starting at 9 on the y-axis represent a set of 60 random human genes as a comparison, and the gray curve represents the global surface temperature (°C) from 66 MYA to present. Compared to cancer-associated genes, primate or human de novo genes have more recent emergence times. Peaks of gene emergence occur in recent 13 MY, during the consistent cooling in Late Miocene that continues to today. Specifically, more than half of the nonrandom genes are estimated to have emerged within recent 10 MY. This result is consistent with Tautz and Domazet-Lošo (2011). The peak of emergence of random genes around 12 MYA occurs earlier than the nonrandom genes around 6–10 MYA, possibly indicating that literature reported de novo genes and cancer-associated genes both have later origins compared to general human genes.

Fig. 3.

Estimated number of emerged human genes and temperature change associated with time. Purple markers represent the estimated number of emerged human genes in a 180 random gene set, orange markers represent the estimated number of emerged human genes in a 60 random gene set, and the gray curve represents the global surface temperature (°C) from 66 MYA to present. As illustrated, the emergence time of 180 random human genes has different peaks than the 60 random human genes, but the overall trend of emerging peaks (around 12 and 10–9 MYA) preceding the peaks of nonrandom genes is not affected by the size of random set.

Fig. 4.

Estimated number of emerged human genes overlayed on temperature change associated with time. Note that the y-axis range is different from Fig. 2. Green markers represent primate or human de novo genes obtained from (Evans et al. 2006; Li et al. 2010; Wu et al. 2011; Xie et al. 2012; Suenaga et al. 2014; Wang et al. 2014; Chen et al. 2015; Ruiz-Orera et al. 2015; Zhang et al. 2015; McLysaght and Hurst 2016; Kalebic et al. 2018; Suzuki et al. 2018; Sun et al. 2020; Yang et al. 2020; Saber et al. 2021), as well as cancer-associated genes obtained from Cancer Gene Census (Sondka et al. 2018). Orange markers represent a random set of 60 human genes as a comparison to the nonrandom genes. The gray curve represents the global surface temperature (°C) from 66 MYA to present. Peaks of gene emergence occur in recent 13 MY, during the consistent cooling in Late Miocene that continues to today, being consist with Tautz and Domazet-Lošo (2011).

Fig. 5.

Estimated divergence time of genus Pan. The vertical dark green line shows the estimated divergence time, and the green area shows the estimated range of divergence time synthesized from literature. While the overall temperature is declining, the estimated species divergence and gene emerging time falls at local warming periods.

Fig. 6.

Estimated divergence time of subfamily Cebinae. The vertical dark green line shows the estimated divergence time, and the green area shows the estimated range of divergence time synthesized from literature. While the overall temperature is declining, the estimated species divergence and gene emerging time fall at local warming periods.

Fig. 7.

Estimated divergence time of subfamily Homininae. The vertical dark green line shows the estimated divergence time, and the green area shows the estimated range of divergence time synthesized from literature. While the overall temperature is declining, the estimated species divergence and gene emerging time fall at local warming periods.

Fig. 8.

An estimated emerging time of 10 genes out of 77. This is the estimated divergence time between {Trachypithecus francoisi} and {Rhinopithecus roxellana, Rhinopithecus bieti}. The vertical dark green line shows the estimated divergence time, and the green area shows the estimated range of divergence time synthesized from literature. While the overall temperature is declining, the estimated species divergence and gene emerging time fall at local warming periods.