Abstract The causes of disappearance of the Neanderthals, the only human population living in Europe before the arrival of Homo sapiens, have been debated for decades by the scientific community. Different hypotheses have been advanced to explain this demise, such as cognitive, adaptive and cultural inferiority of Neanderthals. Here, we investigate the disappearance of Neanderthals by examining the extent of demographic changes needed over a period of 10,000 years (yrs) to lead to their extinction. In regard to such fossil populations, we inferred demographic parameters from present day and past hunter-gatherer populations, and from bio-anthropological rules. We used demographic modeling and simulations to identify the set of plausible demographic parameters of the Neanderthal population compatible with the observed dynamics, and to explore the circumstances under which they might have led to the disappearance of Neanderthals. A slight (<4%) but continuous decrease in the fertility rate of younger Neanderthal women could have had a significant impact on these dynamics, and could have precipitated their demise. Our results open the way to non-catastrophic events as plausible explanations for Neanderthal extinction.

Citation: Degioanni A, Bonenfant C, Cabut S, Condemi S (2019) Living on the edge: Was demographic weakness the cause of Neanderthal demise? PLoS ONE 14(5): e0216742. https://doi.org/10.1371/journal.pone.0216742 Editor: Michael D. Petraglia, Max Planck Institute for the Science of Human History, GERMANY Received: January 10, 2019; Accepted: April 27, 2019; Published: May 29, 2019 Copyright: © 2019 Degioanni et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability: All relevant data are within the manuscript. Funding: The authors received no specific funding for this work. Competing interests: The authors have declared that no competing interests exist.

Introduction The Neanderthals, a human metapopulation that lived between 250,000 and 40,000 yrs ago (OIS 7–3), is arguably the best known human fossil group. Since the discovery of the first Neanderthal specimens in 1856, their origin, evolution, differentiation, variability and genetics have been intensively studied. We have come to the understanding that the Neanderthals emerged from the European branch of Homo heidelbergensis [1–5] and that their differentiation in Europe has been the result of a long evolutionary process [6–8]. Neanderthals, who were the only humans on the European territory, disappeared during the OIS 3, when Homo sapiens arrived. The causes of Neanderthal disappearance fueled a vigorous scientific debate and a number of hypotheses have been put forward to account for their demise (for a recent review see [9]). Because the Neanderthals disappeared at a time when Homo sapiens colonized Europe, their extinction has been related to the expansion of Homo sapiens. According to the most commonly accepted hypothesis, the Neanderthals would have competed with Homo sapiens for food resources and the replacement of Neanderthals would have been favored by Homo sapiens' greater technical skills [10,11], their greater cognitive abilities [11–15], Neanderthal’s narrower diet [16,17] and lower social capacities and network [11,18–21]. However, some prehistorians dispute the superior capacities of the first Homo sapiens in Europe compared to Neanderthals [20,22–27]. In light of our current knowledge about European colonization of the Americas in modern times, some authors have suggested that the disappearance of Neanderthals was also brought about by violent confrontations between the two populations [28,29] and by the exposure to new infectious agents [30–33]. Another hypothesis relates to climate changes affecting Europe during the period of the Neanderthal demise [34–37]. At the time of Neanderthal differentiation, Europe was characterized by a particular environment that underwent large climatic fluctuations, some of which were of a great magnitude with potential consequences for the expansion and/or reduction, and fragmentation of the Neanderthal metapopulation. Although Neanderthals had been coping with marked changes in climate and an associated turn-over in available food resources for almost 200,000 yrs [38,39], they failed to survive after the arrival of new hunter-gatherers, Homo sapiens. All of these hypotheses, however, share the weakness of a much overlooked process of Neanderthal demography in its interaction with the changing environment. For instance, a small population size could have facilitated the replacement or the absorption of Neanderthal by Homo sapiens. Due to the lack of data, very little is known about the demography of past Neanderthal populations. Recent paleo-genetic studies have however estimated [23,40–45] the effective population size (index of genetic variability and not the census size). In spite of the fact that researchers agree on the “small size” of the Neanderthal population [2], its precise and accurate estimation remains difficult. Attempts on the basis of demographic modeling applied to Neanderthals proposed for the entire Neanderthal population (European and Asian) a maximum number of 70,000 individuals [46]. In this paper we are interested in understanding “how” Neanderthal disappeared. We explored qualitatively the possible cause of the Neanderthal population demise in terms of demographic changes, involving above all a reduction in its size. In the absence of palaeodemographic data regarding Neanderthal populations, we used demographic models to search for what values of demographic parameters could have maintained a demographically stable population. In a second step, we altered these values to quantify the necessary change in demographic parameters leading Neanderthals to extinction over a period of 10,000, 6,000 and 4,000 yrs i.e. within a time frame compatible with the known history of modern humans in Europe. In order to make our model more likely, the demographic parameters used are not stable over such a long time, but they change stochastically every year. In particular, we focused on the effect of a fertility reduction for primiparous females known in large mammals to be one of the first demographic rates affected by environmental variation (see [47–49]). Then we also examined the effects of reduced survival rates of different age-classes on extinction probability and time to demise. We started by projecting the effect of a reduction in survival of the youngest children, and finally studied two catastrophic scenarios: the situation of an epidemic and a war scenario, both of which would affect survival rates of adult individuals. Modeling Neanderthal population dynamics To study how Neanderthals disappeared, we modeled their population dynamics with stochastic, age-structured matrix models [50,51]. This is a female-oriented model, where the demographic rates of males are supposed to mirror those of females. We also assumed that males are not a limiting factor for female reproduction, which is generally the case among polygynous species [48,52]. An important characteristic of long-lived species, i.e. species with a long life-expectancy, is the marked age-structure of its demographic rates [53]. For instance, populations of Homo sapiens [54], apes [52], mammalian large herbivores [49] and carnivores [55,56] or seabirds [57] all show a strong age-specific pattern of survival, with low survival rates during the juvenile stages, high survival of prime-aged individuals, and decreasing survival rates once the onset of senescence is reached (see [53] for a review). In the case of Neanderthals, we defined survival rates (Ф) for 5 age-classes: less than 1 y.o. (infant stage), from 2 to 15 y.o. (childhood), from 16 to 18 y.o. (sub-adults), from 19 to 29 y.o. (prime-aged adults) and over 30 y.o. (old). In this latter age group we find the maximum longevity [46]. We know that the longevity of Neanderthals could have been quite extensive [58–60] but, because of menopause, we assumed that the contribution of older individuals to the population growth rate was negligible and would not change our results while increasing the matrix dimension, and hence the calculation time. We set the earliest age for first reproduction of women Neanderthals to 18 y.o. Like survival rates, fertility varied with age, being lower for women aged between 18 and 20 y.o (primiparous) and higher for women between 21 and 30 y.o. (see below for details). We accounted for the spatial-structure of the European Neanderthal populations as revealed by recent genetic analyses [61]. We considered three discrete subpopulations labeled from West to East A, B and C (Fig 1) allowing for movements of individuals and for different demographic rates among subpopulations. PPT PowerPoint slide

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larger image TIFF original image Download: Fig 1. Spatial distribution and location of the 3 Neanderthal subpopulations. Southern Europe (labeled A in green), Northern Europe (labelled B in yellow), and Eastern Europe (labeled C in purple) according to [61]. The full demographic model we used to simulate Neanderthal population dynamics was composed of three sub-models corresponding to each of the identified sub-populations. We included a migration parameter (noted ψ) to allow for individuals to move from a sub-population to another. https://doi.org/10.1371/journal.pone.0216742.g001 In our models, only individuals aged between 16 and 18 y.o., could migrate from one subpopulation to another. The rate of migrating Neanderthals varies among the three subpopulations and is asymmetric, immigration being different from emigration for a given subpopulation [61]. This movement pattern reflects the environmental and social constraints associated with the colonization of Western Europe by modern humans from the East [62,63].

Discussion The main difficulty when working with Neanderthals is the scarcity of empirical data to reliably test the several hypotheses that could account for their disappearance. From a demographic point of view, we only know that Neanderthals existed and disappeared at some point in the past, but we do not know why they disappeared and how long it took for them to become extinct. Either a single or several events might have come into play. These constraints led us to formulate very simple models and to explore the expected dynamics with plausible values of fertility, survival and migration for human populations. For instance, we disregarded a combination of demographic parameters leading to very low extinction probability because this clearly did not occur. For the few empirical data we have, like population size or the time of extinction, the accuracy of the estimates is very low at best. Nevertheless, our aim here is not to evaluate accurate estimates of demographic parameters, but to explore the range of possible values that can generate a decreasing trend in Neanderthal populations. We showed that, in the long run, a slight change in the fertility rate of younger females could have had a dramatic impact on the growth rate of the Neanderthal metapopulation and thus on its long-term survival, in agreement with the observed extinction of Neanderthals within a 10,000, 6,000 or a 4,000 years period. Our modelling suggests that it is not necessary to explain the decrease in size of the Neanderthal population on the basis of catastrophic causes (diseases, extreme climatic events, and disasters such as volcanic eruptions. . . .) or even of the direct or indirect intervention of sapiens. By lowering the average fertility rate from 0.141 to 0.137 for "primiparous reproduction", the population dynamics of Neanderthals switches from a stable or sometimes increasing population to a decreasing population in time which, on the average, eventually dies out over a period of 10,000 yrs,. If the average fertility rate is slightly reduced to 0.135 (or 0.130), this disappearance, on the average, is attained in just 6,000 yrs (or 4,000 yrs). This shows that it only takes a slight decrease in resources over a period of some years to cause a decrease in fertility [82]. It is interesting to note that we have modified primiparous fertility only, therefore focusing on a single class of individuals which comprises 10% of the overall female population (according to the stable age-structure of the model). If our modeling exploration cannot identify the origin of a decrease in fertility of young women, at least putative mechanisms can be put forward: food stress. Because the amount of stored body fat influences fertility in women [82] a decline in resources (caused by climate degradation or competition with sapiens) may affect fertility mostly for young women giving birth for the first time. This hypothesis is consistent with the analyzes of exploitation of the bones of fauna carried out in the South of France [83] that indicate that Neanderthals could have been nutritionally stressed. Besides, although our study is focused on women, disappearance of males could be linked to women fertility. If little is known about the contribution of Neanderthal women to the retrieval of food resources for the group [84], the male contribution was crucial for the group survival. A significant loss of men due to inter-individual conflicts or during hunting activities would have been of great importance for their physical condition, and hence for female Neanderthal fertility. Neanderthal reproductive decline could be amplified by Homo sapiens. Neanderthals and Homo sapiens experienced some hybridation in Central Asia and in Western Siberia [85–88] and on the European continent, as suggested by anthropological [89–91] and genetic evidence [85,86,92]. This hybridation, although important for sapiens allowing the introgression of several useful alleles (see [93] for a review; [45,85]) concerned however a very small number of individuals, since one individual is estimated for every 300 [94] or 250 yrs [95]. Indeed the genetic comparison of the Y chromosome between present-day humans and a Neanderthal of El Sidron [96] suggests that some mutations present in Neanderthals could have caused infertility problems in male hybrids. Such hybrids with less fertility may have contributed to a slight decrease fertility rate [96,97] in Neanderthal population, whereas in sapiens population their high number would have made crossings large enough to lead to the suppression of these deleterious alleles. In agreement with a previous publication [61], we emphasize that we considered a subdivision of Neanderthals among three populations, but given the low Neanderthal population density, we could suppose a stronger fragmentation. Indeed, on the one hand, the three geographical areas considered are wide and heterogeneous from the environmental point of view and, on the other hand, the way of life of Neanderthals as hunter-gatherers corresponds to a clan structure of interconnected individuals [98]. Therefore fragmentation of the metapopulation was probably greater, causing a postponement of their demise [99,100]. By reinforcing demographically the weakest populations on the verge of extinction, the migration process decreased the probability of extinction of the overall metapopulation dramatically, as the theory predicts [101]. Obviously, in the absence of migration, the disappearance of the Neanderthals would have been even more rapid and likely [99,100]. The effects of decreased survival on the extinction probability and time to extinction are considerable as expected for long-living organisms: a decline of less than 1.5% in survival for the youngest children leads to rapid extinction (less than 2,000 yrs), while a reduction of survival rate as small as 0.4% provokes an extinction time of 10,000 years. Another important result of our model is that the disappearance of Neanderthals caused by diseases (infectious and other) contracted by contact with sapiens and leading to a high mortality rate leads to very rapid and sudden extinction. Assuming for instance an infant survival reduced by 10% [102–105]: the demise of Neanderthals would have been much faster than what the archeological records currently suggest. Moreover, owing to the very low Neanderthal density, this hypothesis could account for local disappearances of Neanderthal groups and could not lead to complete demise of the entire population [106]. Similarly, due to the low density of Neanderthals, higher mortality resulting from violence between the two populations could only explain a local decrease in size and extinction, but it would not be applicable to the entire geographical space occupied by Neanderthals. Nevertheless, when exploring this hypothesis, from initial value by reducing adult survival by 10% (keeping all other parameters identical), the whole of the Neanderthal population became suddenly extinct (Fig 3B). Our results lead us to the conclusion that the size of the Neanderthal population could have slowly and gradually decreased over time and that when it was already small and began to decline, Homo sapiens may well have simply taken advantage of an already low density of Neanderthals in order to settle into Europe. As proposed for the Iberian region [107] a low growth rate can be at the origin of Neanderthal disappearance. Our model can make possible to better understand Neanderthal demise at the level of the entire territory and to identify the role of each demographic parameters in this process. Modeling is shown to be a useful tool for answering the question concerning the disappearance of this population on such a huge geographical space as Europe, Asia and the Near East and at a time that is not yet exactly known.

Acknowledgments The authors wish to thank Stéphane Renault for Fig 1 realization and Jeffrey Andrew Barash for his help in editing the manuscript in English.