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The evolutionary origins and consequences of human-commensalism in Passer sparrows

Periodic Reporting for period 1 - EVOSPARROW (The evolutionary origins and consequences of human-commensalism in Passer sparrows)

Reporting period: 2018-09-01 to 2020-08-31

Human activity has altered the evolution of a huge number of species. Some species however are able to adapt, survive and persist to the world that we created. Most notable among these are human commensal species, animals which are dependent on human resources but have arisen without any active intervention from humans. There are widespread examples – rats, mice, microbes and lice. Despite the familiarity of these species to us, we know surprisingly little about the evolutionary origins of human dependent relationships. We also don’t have a good appreciation of the impact that such relationships have on the biology of the animals involved.

The EVOSPARROW project was designed to address this knowledge gap and to examine human commensalism in an evolutionary framework. The project focuses on a familiar, charismatic group of species – Passer sparrows. These include the house sparrow (P. domesticus), a widespread and well-known human commensal bird species. Sparrows were chosen because they are closely associated with humans and there is a good foundation of biological knowledge on them. Furthermore, recent research efforts have established genomic tools that make it possible to investigate the provenance of this widespread bird.

The overarching aim of EVOSPARROW is to investigate how commensalism arose in Passer sparrows and to investigate the evolutionary consequences this shift to a human dependent niche has had on the species. Using genomic and phenotypic data, the project aimed to disentangle the evolutionary history of Passer species, reconstruct the evolutionary history of Passer sparrows in Europe and finally identify the genomic basis of phenotypes involved with adaptation to a human commensal life history.

Human commensal species can have profound effects on human society. For example, commensalism may be a pathway to domestication (i.e. dogs) or may lead to the development of pest species such as mice. Investigating commensalism in an evolutionary context has two major values to society. Firstly, an understanding of the origin of such species and the traits that allow them to adapt to human environments can provide important insight into methods for managing their impacts. Secondly, the history of these species are often closely entwined with our own – by piecing together how these species came to be, we are also able to reflect on major transitions and changes in human society.
As a result of EVOSPARROW, we have sequenced the genomes of 412 sparrows from across the distribution of the genus. This includes 18 different species (65-94% of extant species, depending on the authority) from which we have been able to construct a high-resolution, genome-wide phylogeny. This phylogeny allows us to place the evolution of human commensalism in Passer sparrows in proper evolutionary context. Intriguingly, the results from this work suggest that human commensalism has likely arisen at least four times independently within the Passer genus.

The large-scale population genomic dataset generated by EVOSPARROW has been analysed to investigate population structure and demographic history of Passer species in Europe. In particular initial results suggest that the house sparrow did likely spread into Europe from Central Asia and the Middle East with early agriculturalists during the Neolithic. This has likely resulted in significant gene flow between the house sparrow and the Spanish sparrow, a wild species already present in Europe.

Using a collection of sparrow skulls available at the University of Oslo and also a private collection from Iran, EVOSPARROW investigated the morphological diversity associated with a human commenal niche. Scanning using microCT produced high resolution 3D scans which allowed detailed analysis for beak and skull shape. Initial results strongly indicate a change in beak and craniofacial morphology between commensal and non-commensal lineages, as well as significant change in brain case size.

A comparative genome scan between the house sparrow and a non-commensal subspecies, the Bactrianus sparrow shows signatures of selection across the genome. These suggest a positive selective sweep has occurred in the house but not Bactrianus sparrow and demographic modelling indicates these subspecies diverged within the last 10,000 years. Selection scans indicate a number of promising candidate genes for adaptation to a human niche, including COLL11A1, a gene involved in craniofacial development and AMY2A, an amylase gene that is involved in starch digestion in humans and dogs.

Work is continuing on the results of the EVOSPARROW project. Although no publications have been published as a direct result of the project yet, a major manuscript summarising the main findings is in preparation with a deadline for submission by Sept 2020. The findings of the project have been presented at three international conferences and a large number of departmental seminars.
The results of the EVOSPARROW project have formed the basis of a wider research program to examine the evolutionary basis of human commensalism. New research funding is being applied for on the basis of these results and we aim to investigate the phenomenon in a wider range of species, particularly on a macroevolutionary scale.
EVOSPARROW has shown that the four human commensal Passer species are evolutionary independent