Creationism in Crisis - The Evolution of African Primates

Cercopithecus diana

Complex Evolutionary History With Extensive Ancestral Gene Flow in an African Primate Radiation | Molecular Biology and Evolution | Oxford Academic

Cercopithecus diana

Mustached guenon,
Cercopithecus cephus

De Brazza's guenon,
Cercopithecus neglectus

Stuhlmann's Blue monkey,
Cercopithecus mitis stuhlmanni,

Crowned Guenon
Cercopithecus pogonias

12 years ago, I wrote a blog post to explain why, because speciation is a process, not an event, we often don't even know it's happened until well after the event when we can see we have a new population with distinct characteristics. I illustrated this with a hypothetical example of monkeys in a forest being split into isolated populations by climate change.

In it I said:

But, gradually, due to climate change or continental drift, or maybe a change in ocean currents, the forest begins to get drier and turn into grasslands, with trees surviving only close to rivers. In other words, the monkey population is broken up into isolated groups which can no longer interbreed because they simply don't come into contact any more. Each group will be free to evolve according to the local conditions in its woodland. Eventually, maybe after a few hundred thousand years, maybe a million or two, these groups may evolve to the point where they not only look different to each other but may not be able to interbreed even if they do meet up.

So where and what was the 'speciation event'? At what point in the process could an observer say, "Hey! I've just seen speciation occur! It happened when...". In fact, we only know that speciation has occurred retrospectively because, according to our rules of taxonomy, failure to interbreed means they are now different species. Maybe if we had been able to examine them a hundred thousand years ago we might have found that they could still interbreed. Maybe we would have found an incompletely speciated 'ring species'.

There was no sudden emergence of a new species; no sudden branching of the 'tree of life'; no mutation which brought a new species into being and no 'macro-evolution' event. There was no event which creation pseudo-scientists proclaim to be impossible and which they claim has never been seen. All there was was a slow accumulation of difference, directed by natural selection with each group doing nothing but struggling to survive and reproduce with the ones which left the most descendant contributing the most genes to the gene-pool.

Now, take the same scenario, only this time the climate changed again after a few tens of thousands of years and the isolated scattered groups could once again mix freely. But this time maybe they had not diverged sufficiently to prevent interbreeding, or maybe one group now had a significant advantage over the others. In these cases, the group with the genes which gave them greater success would come to dominate and possibly replace the others.

Is this speciation? Is this the point at which we can say a new species arose and the 'archaic' form went extinct? Or is this merely evolution of the entire species? Were those groups isolated for a few thousand years new twigs on the monkey branch of the tree of life, or were they merely groups of individuals with the potential to become new species, but which never quite made it? Certainly, the day they came back into contact, nothing happened to their genes. It was not a change on their part which caused them to re-establish contact. It was the environment which changed.

Rosa Rubicondior: Evolution - Making a Monkey (4 July 2012)

And now, as though to confirm my hypothetical example was close to the real thing, a team of archaeologists and geneticists, led by Axel Jens and Katerina Guschanski of the Department of Ecology and Genetics, Animal Ecology, Uppsala University, Uppsala, Sweden, have carried out a whole genome analysis of 22 species of West African guenons (monkey of the Cercopithecini tribe - one of the world's largest primate radiations) and shown how the different species diverged with frequent gene flow across species boundaries and hybridization events playing a part in the process of radiation and diversification.

The team have published their findings, open access, in the journal Molecular Biology and Evolution. In it they say:

Abstract

Understanding the drivers of speciation is fundamental in evolutionary biology, and recent studies highlight hybridization as an important evolutionary force. Using whole-genome sequencing data from 22 species of guenons (tribe Cercopithecini), one of the world's largest primate radiations, we show that rampant gene flow characterizes their evolutionary history and identify ancient hybridization across deeply divergent lineages that differ in ecology, morphology, and karyotypes. Some hybridization events resulted in mitochondrial introgression between distant lineages, likely facilitated by cointrogression of coadapted nuclear variants. Although the genomic landscapes of introgression were largely lineage specific, we found that genes with immune functions were overrepresented in introgressing regions, in line with adaptive introgression, whereas genes involved in pigmentation and morphology may contribute to reproductive isolation. In line with reports from other systems that hybridization might facilitate diversification, we find that some of the most species-rich guenon clades are of admixed origin. This study provides important insights into the prevalence, role, and outcomes of ancestral hybridization in a large mammalian radiation.

Introduction

Ancient hybridization has been reported in many organisms, including mammals (Taylor and Larson 2019). However, owing to their large genomes, studies of entire mammalian radiations, particularly among species-rich groups, are underrepresented (but see Gopalakrishnan et al. 2018; Chavez et al. 2022), and most cases focus on pairs of species (Taylor and Larson 2019). Yet, large radiations with lineages of different ages offer a unique opportunity to understand how increasing lineage divergence along a speciation continuum may impact the ability to hybridize and the outcome of hybridization events. As reproductive isolation accumulates with genetic distance (Coyne and Orr 2004), the impact and consequences of introgression may vary, as well as the mechanisms that allow for genomic incompatibilities to be overcome. Several studies have reported that introgression between divergent lineages may spark rapid speciation and adaptive radiations by introducing novel genetic variation (Meier et al. 2017; Marques et al. 2019.1; Svardal et al. 2020). Comprehensive genomic datasets from species-rich radiations offer unique possibilities to study the interplay between hybridization, adaptation, and speciation.

Here, we focus on guenons (tribe Cercopithecini), a species-rich group of African primates that radiated over the last ca. 10 to 15 million years (MY) (Guschanski et al. 2013; Kuderna et al. 2023). With 89 taxa and over 30 distinct species (IUCN 2022.1), guenons represent one of the world's largest primate radiations, spanning a broad range of divergence times. Guenons are renowned for their ecological, morphological, and karyotypic diversity and have attracted the attention of evolutionary biologists and ecologists for decades (Dutrillaux et al. 1988; Glenn and Cords 2002; Grubb et al. 2003; Enstam and Isbell 2007; Moulin et al. 2008). Yet, despite possessing multiple characteristics that act as reproductive barriers in other study systems, guenons readily hybridize, even across deep evolutionary distances (Detwiler et al. 2005; de Jong and Butynski 2010; Detwiler 2019.2). For example, Detwiler (2019.2) reports viable and at least partially fertile hybrids between Cercopithecus mitis and Cercopithecus ascanius, 2 species that diverged ca. 5 million years ago (MYA) (Kuderna et al. 2023) and differ in chromosome numbers. Genomic studies have also identified ancient gene flow in several guenon lineages (Svardal et al. 2017.1; van der Valk et al. 2020.1; Ayoola et al. 2021), but the extent and role of ancestral hybridization throughout the clade is unknown.

As such, guenons provide a highly informative system to study the evolution of reproductive isolation and speciation in the context of a large radiation. Specifically, we aim to (i) study genomic patterns of introgression and mechanisms that allow barriers to gene flow to be overcome at different evolutionary distances, (ii) investigate the repeatability of introgression landscapes along the speciation continuum and (iii) explore the functional role of introgressed regions and identify loci contributing to reproductive isolation.

Taxonomy, species richness and mitonuclear discordances among guenons. (A) Taxonomic overview of the 22 species included in this study, shown according to genus and species groups. The color of the vertical bars corresponds to branch colors in (C). (B) Species richness/degree of sympatry for species included in this study, based on species distributions from IUCN (2022). (C) Astral species tree obtained from 3,346 autosomal gene trees (left) and maximum likelihood tree constructed with RaxML from complete mitochondrial genomes (right), with connectors highlighting phylogenetic discordances. Node annotations show branch quartet support (left) or bootstrap support (right), where this was <95%. Branches are colored based on genus/species groups as in (A). Tree topologies were estimated from all available samples (supplementary figs. S1 and S7, Supplementary Material online) and were subsequently pruned to a single sample per species prior to divergence date estimates with MCMCTree, applying fossil calibrations to the nodes annotated with asterisks. Nodes were rotated to aid visualization of mitonuclear discordances.

Photo credit for (A): hamlyni: NRowe/alltheworldsprimates.org; diana, Chlorocebus: K. Guschanski; neglectus: M. D’haen; mona: S. Knauf; mitis: M. Mpongo & K. Detwiler; cephus: S. Crawford & K. Detwiler; Allochrocebus: T. Ukizintambara; Erythrocebus: T. Valkenburg; Miopithecus: P. Paixão; Allenopithecus: D. Sutherland.

Axel Jensen, Frances Swift, Dorien de Vries, Robin M D Beck, Lukas F K Kuderna, Sascha Knauf, Idrissa S Chuma, Julius D Keyyu, Andrew C Kitchener, Kyle Farh, Jeffrey Rogers, Tomas Marques-Bonet, Kate M Detwiler, Christian Roos, Katerina Guschanski,
Complex Evolutionary History With Extensive Ancestral Gene Flow in an African Primate Radiation, Molecular Biology and Evolution, Volume 40, Issue 12, December 2023, msad247, https://doi.org/10.1093/molbev/msad247

Copyright: © 2023 The authors.
Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. Open access.
Reprinted under a Creative Commons Attribution 4.0 International license (CC BY 4.0)

So, as I speculated back in 2012, in just such a scenario, there will be alopatric speciation with periods when the diverging species acted like a ring species, and gene-flow and hybridizations between related species.

Creationists now need to explain how the data the research team produced is best explained by a magic creator magicking species of monkey so that they can interbreed and with genomes that just happen to look like they diverged from a common ancestor 10-15 million years ago and some members of one species having the same mitochondrial DNA as another. The theory of evolution of course provides a perfect explanation for this data as I showed by predicting 12 years ago that this would be the cause of a radiation of monkey species.

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