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Genomes, food and microorganisms in the (pre)history of cat-human interactions

Periodic Reporting for period 2 - FELIX (Genomes, food and microorganisms in the (pre)history of cat-human interactions)

Okres sprawozdawczy: 2022-10-01 do 2024-03-31

The transition from hunting-gathering to farming that started about 11,000 years ago (ya) represented one of the most dramatic changes in human prehistory, marking the rise of the Neolithic era. A result of the impulse of humans to manage and exploit nature, the influence of domestication on our culture, biology and ecology has been paralleled to key events that made us humans, such as the invention of stone tools, religion, written language, and mathematics.
In recent years, biomolecular archaeology has significantly contributed to the understanding of the domestication process. In particular, ancient DNA (aDNA) and chemical dietary signatures of stable isotopes retrieved from archaeological animal remains have become crucial analytical tools to track cultural and economic transitions as well as migratory shifts in human (pre)history. The spotlight of this interdisciplinary research has so far been focused mostly on humans, and, secondly, on livestock species (cattle, pigs, sheep and goats), dogs and horses. However, one of the most popular pets in present-day society remains largely understudied at the multi-disciplinary level, the domestic cat (Felis catus). This creates a significant gap of our knowledge concerning this important species and the overall understanding of animal domestication.

Cats are enigmatic domesticates (and one would even argue whether they are domestic at all). Pest-control agent, object and symbol of value in past civilizations, companion animal, and iconic celebrity of the web in the modern society, the cat has long held a unique position in our collective consciousness, and nowadays it is together with the dog the most popular pet in the world. Yet, its domestication process is still poorly understood. Filling this gap of knowledge will complement the evidence already gathered for species more extensively studied, adding key information to the debate around animal domestication.
Cats and humans had a long history of commensalism characterized by a gradual intensification of their relationship, which transformed cats from pest-control agents into human companions. In no other species as the cat, domestication has led to profound changes in an animal’s behavior, yet not paralleled by a wide spectrum of morphological variation. In this regard, cat domestication is unique and unconventional in its kind and may offer novel paradigms for advancing our understanding of animal domestication.
The domestic cat was never primarily exploited for its economic or subsistence value, however, the intimate bond with humans made it one of the most successful species in nature, which spread from the original place of domestication in the Near East and North Africa globally in all continents except Antarctica. Understanding how cats adapted to the anthropogenic niche across time and space will provide unprecedented evolutionary insights on domestication and human-animal interactions.
The evolutionary success of the cat is unquestioned, yet as highly invasive species, this comes at significant cost to native prey fauna and wildcat populations, with strong ecological and conservation implications. Furthermore, nowadays a large part of the domestic population lives indoors, in close contact with humans, posing significant economic and public health burdens in modern societies associated with the spread of zoonotic diseases.

By implementing state-of-the-art bioarchaeological methods, FELIX will dig deeply into the history of cat domestication. It will test to what extent and when the increasing bond with humans changed the cat genome, and how cats adapted to anthropized ecosystems, with particular regard to feeding strategies. It will tackle fundamental and yet unexplored questions on the significant toll left by cat domestication on human populations, zoonotic diseases, an unprecedented effort that has been so far applied only to ancient humans. To do that, FELIX will reconstruct the history of cat-human relationships through the multidisciplinary lens of three fundamental variables strongly influenced by domestication: genomes, food, and microorganisms.
By reconstructing full genomes of ancient cats, FELIX aims at unravelling the times and places of cat dispersal, with a peculiar focus on understanding the role of Neolithic farming communities from the Levant and the Egyptian civilization in the history of cat domestication. FELIX will pinpoint how the increasing bond with humans across a wide spectrum of socio-cultural contexts, from prehistoric farming communities to ancient Egyptian and Medieval societies, shaped the cat genome, leading to behavioural changes that transformed cats into pets. By analysing stable isotopes from bone remains FELIX will also examine how cats changed their nutritional behaviour while adapting to anthropized ecosystems, for example the consumption of fish and cereal-based food. Finally, FELIX aims at retrieving the DNA of ancient microorganisms from archaeological remains, with the objective to document the temporal trajectories of pathogen infections in cats. This will offer unprecedented insights on the spread of zoonotic diseases and will raise public awareness on the role of the cat as cherished pet, but also as one of the world’s most invasive alien species in natural ecosystems and host of infectious diseases recognized today as public health threats.
FELIX has been able to gather so far archaeological samples of 1302 archaeological wild and domestic cats covering the last 15 millennia in Europe, North Africa and West Asia.
With regards to the implementation of the first line of investigation, Genomes (ancient DNA analysis to investigate full mitochondrial DNA (mtDNA) and genome-wide data), the members of the team have processed so far 336 ancient samples from Europe, the Near and Middle East and North Africa. This made it possible to generate 86 complete mtDNA genomes and 30 low-coverage nuclear genomes.
For the second line of investigation, Food (extraction of collagen and carbon, nitrogen and hydrogen stable isotope analyses), we have been able to shed further light on cats' trophic ecology and their commensal relationship with humans by measuring carbon and nitrogen stable isotopes chemical signals in hundreds of cats from Northern Europe (Krajkarz et al. 2022) and the Middle East (Brozou et al. 2023).
We have also explored in the third line of investigation, microorganisms, the pattern of microbial DNA preservation in more than 200 archaeological cats. We were able to detect DNA molecules of potential pathogens (amongst which Toxoplasma gondii) and further investigation is currently being addressed to demonstrate the authenticity of these results and elucidate the challenges associated with potential ancient environmental contamination.
The behavioural features of the Near Eastern wildcat (F. s. libyca), more tolerant of human presence, and the cultural conditions of the Neolithic, represented the perfect mix to spark the start of the cat-human relationship. However, a stronger shift in this interaction may have occurred later in Egypt. The peculiar social and cultural context of the Egyptian society may have facilitated the evolution of a more tolerant disposition of cats towards humans through selection for docility. From pest-control agents in farming communities, cats of Egyptian households probably turned into the companions that we know today. The increasing popularity of cats among Mediterranean cultures (the Phoenicians, Carthaginians, Greeks, Etruscans, and Romans) and their usefulness on ships infested with pests presumably sparked their dispersal across the Old World from Egypt.
Biomolecular archaeology offers the tools to address these unanswered questions. In particular, the technological advance in sequencing techniques of the last decade has paved the way to the paleogenomic era. Exploring at the high resolution of full genomes the genetic variation at different time points has succeeded in reconstructing evolutionary scenarios previously hardly imaginable, first and foremost for the human species. Through cutting-edge DNA sequencing techniques, FELIX is reconstructing ancient genomes of hundreds of wild and domestic cats from the last 15 000 years across a wide geographic range encompassing the Eurasian and African continents. It
will shed further light on the dispersal of cats from the Near East and Egypt during the last 10 000 years. It will seek to define to what degree domestic cats interacted with local wildcat populations upon arrival in novel areas along with humans. By opening a window onto the past genetic variation of cats in various natural and anthropogenic contexts, including ancient Egyptian mummies, FELIX will understand how cats turned into the pet that we know today.
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