Rhino: Horn of Discord

How many horns does a rhinoceros have? The question may seem harmless. However, the answer made the classification of rhinos an unsolvable mystery for a long time…until recently. This answer is simple: of the five current species, some have one horn, others have two. But things get more complicated when we look at the geographic distribution of these species. white rhinoceros in africa (Ceratotherium simum) and black rhino (Diceros bicornios) have two horns. On the Asian continent, the Indian rhinoceros (Rhino unicorn) shows only one. On the other hand, the two species from the Sunda Islands in Indonesia bear little resemblance to each other. javan rhinoceros (Rhino Sondaicus) has one horn, while Sumatra has (Dicerorhinus sumatrensis) has two. Thus, classifying these five species by geographic distribution or number of horns does not produce the same result. How to establish their phylogeny?

One horn, two horns, three hypotheses

Three hypotheses have been put forward. And they all lead to a great phylogeny. In 2010, Pierre-Olivier Antoine, a paleontologist at the University of Montpellier, and colleagues proposed a “horn” hypothesis that links two African rhinoceros with the Sumatra rhinoceros. Based on morphology, this was confirmed at the time by genetics and later by analysis of tooth enamel proteins. But last year, along with other colleagues, Pierre-Olivier Antoine this time defended a geographic hypothesis uniting all Asian rhinos based on morphoanatomical research, new genetic analyzes and comparative sequences of collagen from living and extinct animals, one of several proteins extracted from fossils. In the meantime, however, Thomas Gilbert of the University of Copenhagen, Denmark, and colleagues have published an analysis of mitochondrial DNA (found in mitochondria, the energy factories of cells) that distinguishes the Sumatran rhinoceros from all others, placing it as a sister group to the other four species. How to distinguish the correct hypothesis?

These conflicts show that the consistently used symbols are of low resolution, i.e. not enough to choose between hypotheses. So Thomas Gilbert assembled a strike team that included leading researchers on the subject, including Pierre-Olivier Antoine, to find a high-resolution character set that would allow for a reliable phylogeny.

Paleontologists first added three late Pleistocene fossil species (between 126,000 and 11,700 years ago) to the equation: the Siberian unicorn (Elasmotherium sibiricaone horn), Merck’s rhinoceros (Stephanorhinus kirchbergensistwo horns) and a woolly rhinoceros (Coelodonta antiquitatis, two horns). All Eurasian, but also of unclear phylogenetic position…

Then, knowing that Donald Primerano’s team at Marshall University in the US had just sequenced the genome of the Sumatran rhinoceros, Thomas Gilbert’s team turned to phylogenomics, a classification based on the study of whole genomes. She began by sequencing the complete genomes she lacked: the genomes of two current rhinos and three fossils, a technical feat in itself. Then, adding the horse and tapir genomes as an outgroup, she constructed a phylogeny in which, thanks to the temporal calibration provided by the fossils, she dated speciation.

Result: preference is given to the geographical hypothesis. From an ancestor that lived in Eurasia, the first speciation 35 million years ago gave rise to the Siberian unicorn, which populated most of western Russia. Then, between 16 and 15 million years ago, at the end of the Lower Miocene, during a pronounced climatic optimum (between 17 and 14 million years ago, the temperature was 3-4 ° C higher than today), a massive diversification occurred. brought two species to southern Africa, while the rest remained in Eurasia. Paleontology has perfectly documented this period, when many animals – giraffes, svinoids (warthogs …), viverrids (civet …) – immigrated to Africa, while others – monkeys, elephants – emigrated to Eurasia. Then Woolly and Merck rhinoceroses invaded the entire continent, while Southeast Asia was home to a special plantation from which a single-horned branch emerged.

© Liu S. et al., Cell, vol. 184, p. 4874-4885, 2021 (CC BY 4.0)

This phylogeny explains why the Sumatran rhino used to be so hard to find. It is isolated unless fossils are included, but this situation can lead to phylogenetic reconstruction artifacts. In addition, a detailed analysis of genomes revealed the flow of genes between species through hybridization. Then we realize that phylogenies built from parts of genomes gave rise to various trees.

Inbreeding doesn’t explain everything

The icing on the cake, as is often the case, is whole genome sequencing, which has yielded unexpected insights. First, it provided the basis for assessing the genetic diversity of extinct and modern rhinos. Geneticists have long noted that the genetic diversity of modern rhinos is very low, which is attributed to the erosion of populations, which would lead to significant inbreeding. But new results show that already in extinct species, the genetic diversity of the rhinoceros family was low compared to other herbivores and some carnivorous mammals. However, since the populations of herbivores are larger than those of carnivores, we would expect much more genetic diversity in the former than in the latter. This surprising result is important for conservation biology because it shows that the recent decline in the rhinoceros population has had less of an impact on genetic aspects than previously thought.

Then, surprisingly, genome sequencing provided an explanation for the curiosity of rhinos, their very poor eyesight. Indeed, genome analysis revealed mutations in the gene IFT43. However, the protein produced by this gene is involved in the intracellular transport of proteins along flagella and cell cilia. What report? The cones or rods of the retina function by accumulating opsins – photoreceptor proteins – in the ciliated part. But the latter play their role only if they bind to the chromophore, retinal, a form of vitamin A. However, without functional transport along the eyelashes, retinal does not attach to opsins. A deficiency in the IFT43 protein in rhinos is thought to be one of the causes of their deplorable vision.

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