Humans created an environment that increased selective pressures on subgroups of those species that became domestic. We propose that the domestication process may in some cases have been facilitated by changes in mating behaviour and resultant sperm competition. By adapting to sperm competition, proto-domestic animals could potentially have outcompeted their wild counterparts in human-constructed niches. This could have contributed to the restriction of gene flow between the proto-domesticates and their wild counterparts, thereby promoting the fixation of other domestication characteristics. Further to this novel perspective for domestication, we emphasise the general potential of postcopulatory sexual selection in the restriction of gene flow between populations, and urge more studies

Hulme-Beaman, Ardern

Searle, Jeremy B

Stockley, Paula

Humans created an environment that increased selective pressures on subgroups of those species that became domestic. We propose that the domestication process may in some cases have been facilitated by changes in mating behaviour and resultant sperm competition. By adapting to sperm competition, proto-domestic animals could potentially have outcompeted their wild counterparts in human-constructed niches. This could have contributed to the restriction of gene flow between the proto-domesticates and their wild counterparts, thereby promoting the fixation of other domestication characteristics. Further to this novel perspective for domestication, we emphasize the general potential of postcopulatory sexual selection in the restriction of gene flow between populations, and urge more studies.</jats:p

Ardern Hulme-Beaman

Jeremy B. Searle

Paula Stockley

Crossref

Biology Letters

Sperm competition as an under-appreciated factor in domestication

University of Liverpool Repository

PAGE  2Sperm competition as an under-appreciated factor in domesticationAuthors: Ardern Hulme-Beaman1,2,*, Jeremy B. Searle3, Paula Stockley4*Corresponding authorAffiliations:1 Department of Archaeology, Classics and Egyptology, University of Liverpool, Liverpool, L69 7WZ, UK ardernhb@gmail.com (​mailto:ardernhb@gmail.com​)2 School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool, L3 3AF, UK3 Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY14853-2701, USA4 Mammalian Behaviour & Evolution Group, University of Liverpool, Leahurst Campus, CH64 7TE, UK AbstractHumans created an environment that increased selective pressures on subgroups of those species that became domestic. We propose that the domestication process may in some cases have been facilitated by changes in mating behaviour and resultant sperm competition. By adapting to sperm competition, proto-domestic animals could potentially have outcompeted their wild counterparts in human-constructed niches. This could have contributed to the restriction of gene flow between the proto-domesticates and their wild counterparts, thereby promoting the fixation of other domestication characteristics. Further to this novel perspective for domestication, we emphasise the general potential of postcopulatory sexual selection in the restriction of gene flow between populations, and urge more studies.Keywords: Sperm competition; Cryptic female choice; Mating behaviour; Speciation; Gene flow; DomesticationIntroductionThe processes involved in prehistoric animal domestication are complex, varied and insufficiently understood [1,2]. The earliest known domestication, dogs from wolves (Canis lupus), preceded metallurgy or crop domestication [3]. It is unlikely that this and other early domestications occurred with the forethought, or even resources, to capture, control and directly breed a viable population of domestic animals. Consequently, increasingly domestication is seen as analogous to natural speciation, involving adaptation to new niches without direct human control [3]. We must therefore consider the behaviour and biology of the progenitor populations of domesticates to better understand the domestication process, because they were likely free-roaming and freely breeding.Both speciation [4] and domestication involve the development of traits that distinguish the emerging ‘taxa’. Central to understanding both processes is identifying how those traits can be maintained (and added to) despite gene flow between the emerging taxa [3]. Although the domestication process was likely enhanced through moving early domesticates beyond the native range of their progenitors [1], the earliest stages occurred with proto-domesticates and their wild progenitors living sympatrically. Therefore, at the origin of domestication, a key question is: how did domestic traits become fixed despite the potential for proto-domestic and wild animals to interbreed? If we argue that a human driven gene flow barrier is unlikely, then a scenario whereby animals diverged due to behavioural traits must be considered (e.g. scavenging of human resources leading to docility towards humans, allowing easier access to those resources) [1]. Behaviourally driven scenarios, with associated novel niche exploitation, have analogies to ‘ecological speciation’ [3,5]. However, a missing element in these behavioural models of domestication is a mechanism by which gene flow might be restricted, other than habitat preference. Here, we propose a possible mechanism for gene flow restriction between wild and proto-domestic animals. We suggest that increases in multiple mating behaviour due to a local increase in population density around humans could augment the domestication process. This mechanism would likely have had the greatest effect on species that underwent domestication with the least active human influence, i.e. the domestication process that we have been emphasising, also described as the ‘commensal pathway’ to domestication [1] (for an overview of the three pathways to domestication see Supplementary Information). Furthermore, the evolution of commensalism per se in anthropogenic environments may be influenced in similar ways [6]. Therefore, we argue that for proto-domestic commensal species, high population density around humans likely promoted increases in promiscuity, with important implications. This increased promiscuity may have resulted in selective pressures on traits for improved fertilisation success in the promiscuous populations, leading to a gene flow restriction mechanism between proto-domestic animals and their wild progenitors, and allowing the fixation of other domestic behavioural traits. Here we briefly outline this overlooked aspect of domestication.Domestication and population densityThree fundamental domestication requirements are: 1) sufficient resources to support both the human society and a population of the animal being domesticated; 2) a local population of proto-domestic animals in close enough proximity to humans to develop familiarisation; 3) sufficient numbers of the proto-domestic animals to form a viable breeding population during familiarisation. Human refuse provides highly localised resources in close proximity to humans that could attract progenitor species for domestication (e.g. wolves, wildcats (Felis silvestris) and wild boar (Sus scrofa) [3]). Use of such resources by wild animals regularly leads to increased local population density, which brings about numerous behavioural changes and selective pressures [6]. Urban red foxes (Vulpes vulpes), feral cats and feral dogs provide analogues: they live locally at high density with a greater number of smaller, more overlapping home-ranges in anthropogenic environments compared to their wild counterparts [7–9]. Direct comparisons with them must be used cautiously as feral populations may harbour vestigial domestic traits. However, the comparison with urban foxes demonstrates such changes in home-ranging behaviour with use of human resources and this is seen with numerous other species [6]. Therefore, these features of ecology and behaviour in response to anthropogenic resources could be considered analogous to the familiarisation phase of domestication [2,3]. The only well-documented study of evolutionary change during domestication, the Farm-Fox Experiment, occurred in highly controlled environments, with frequent interactions between handlers and animals [10]. The proximity and level of interaction required for domestication of a free-roaming and freely breeding population is unknown, but must have been regular and consistent to exert selective pressure over multiple generations. A higher than normal density of proto-domestic animals around humans seems a probable way by which consistent selective pressures could have been exerted by small human populations on free-roaming proto-domestic species. For solitary, monogamous or small breeding unit species, such population density change could result in dramatic behavioural changes.Density, mating behaviour and sperm competitionAs population density increases, males encounter mating opportunities more frequently, and the benefits of pursuing these will likely outweigh the costs of attempting to defend exclusive access to females. Equally, females encounter more potential mates and may gain fitness benefits (or reduce costs of harassment) by mating multiply [11,12]. Polyandrous mating therefore often increases with high population density. For example, house mice (Mus musculus) [13], urban red foxes [14], free-roaming dogs [7] and feral cats [15] all show higher levels of multiple paternity in high-density populations. The evolutionary consequences of polyandry on male reproductive traits are well documented among diverse taxa [16–18]. These include increased sperm production and ejaculate quality, and changes in sperm morphology [19,20], ejaculate composition [21], genital morphology [22] and copulatory behaviour [23]. Adaptations to sperm competition can evolve rapidly [24], leading to marked divergence in reproductive traits of closely related species and/or populations. Increased multiple mating and sperm competition can also drive evolution of female reproductive traits, including gamete evolution [25], through sexual conflict [26] and cryptic female choice [27]. This can lead to rapid coevolution of both sexes’ reproductive traits [28,29], with potential to promote reproductive isolation and speciation [26,30]. We might then predict that with the onset of domestication, and the increase in density of proto-domestic animals around small human settlements or campsites, mating behaviour changes could rapidly change reproductive traits and competitive fertility.Mating behaviour augmenting the domestication processModern domestic species display dramatically different social behaviours compared to their wild counterparts [31], not only in their inter-species interactions (e.g. docility with humans), but also in their intra-species interactions (e.g. increased social tolerance of conspecifics [32]). Increased social tolerance in turn could promote opportunities for polyandrous mating. Therefore, if proto-domestic animals lived at higher density than their wild counterparts, then the likelihood of proto-domestic females breeding with multiple partners would increase (e.g. commensal urban foxes [14]). Then, if proto-domestic females mate with multiple males (wild and proto-domestic), the more abundant and/or higher quality sperm of the proto-domestic males (under selection for sperm competition) would outcompete sperm of wild males. Proto-domestic sperm bias could result in reduced gene flow between proto-domestic and wild populations. As mammalian females generally remain close to their natal home-range [33], domestic traits of proto-domestic populations are less prone to dispersal into wild populations. Sperm competitive traits could spread through wild populations via proto-domestic male dispersal and inter-breeding. However, maintaining adaptations to sperm competition is costly [34], and of little benefit without multiple mating. Hence, while habitat and resource preference probably played a central role in domestication, this form of gene-flow restriction could have intensified the process, helping other domestic traits (such as genetically determined social behaviours [35], and developmental plasticity [36]) to become fixed. It is therefore important to assess evidence of adaptations to sperm competition and corresponding female traits in modern domestic animals, and, where possible, try to identify selective pressures on these traits through time (See Supplementary Information for review of evidence).ConclusionTo fully understand the domestication process, we must consider the behaviour and ecology of the wild counterparts of domestic animals. Habitat preference and selective pressures exerted by humans (whether intentional or unintentional) are likely primary driving forces of the domestication process, but changes in mating behaviour may have played a key role in restricting gene flow and accelerating the process. A greater understanding of the genetic architecture of traits selected for due to changes in mating behaviour, including both male and female reproductive traits, should enable us to track these changes through time. More research is needed, both to explore evidence for increased selection on key reproductive traits through time, and to model their contribution to the domestication process. Examining reproductive traits in modern commensal species may prove particularly useful for understanding density specific reproductive traits. Understanding the extent of changes in the mating behaviour of proto-domestic animals will greatly illuminate the domestication process and the nature of human societies that gave rise to the phenomenon. With the analogy between domestication and speciation, if changes in sperm competition promote domestication, then we should also consider more generally the role of postcopulatory sexual selection in genetic isolation of populations.References1.	Zeder MA. 2012 Pathways to animal domestication. In Biodiversity in agriculture: domestication, evolution and sustainability (ed P Gepts), pp. 227–259. Cambridge: Cambridge University Press. 2.	Vigne J-D. 2011 The origins of animal domestication and husbandry: A major change in the history of humanity and the biosphere. Comptes Rendus - Biol. 334, 171–181. (doi:10.1016/j.crvi.2010.12.009)3.	Larson G, Fuller DQ. 2014 The evolution of animal domestication. Annu. Rev. Ecol. Evol. Syst. 45, 271–295. (doi:10.1146/annurev-ecolsys-120213-091620)4.	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(doi:10.1111/eth.12044)Funding bodiesA.H.B. is funded by a Leverhulme Trust Early Career FellowshipAcknowledgementsWe thank Les Noble, Keith Dobney, Greger Larson, Laurent Frantz, James Haile, Robert Lachlan and two anonymous reviewers for helpful discussions and comments.Author contributionsAHB conceived the project and compiled the evidence; AHB, PS and JBS drafted the manuscript.

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Sperm competition as an under-appreciated factor in domestication

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