Neo-Darwinism,niche construction theory,and the initial domestication of plants and animals

The initial domestication of plants and animals and the subsequent emergence of agricultural economies, which began independently more than 10,000 years ago in a number of different world regions, represent a major evolutionary transition in earth history. It is these domesticates, and the agricultural economies based on them, that have formed the lever with which humans have substantially modified the earth’s terrestrial ecosystems over the past ten millennia. General explanations for this transition from hunting and gathering to food production economies formulated over the past 40 years have been based on standard evolutionary theory (SET) and employ the assumption of unidirectional adaptation—that environments change and species adapt. Here I compare these proposed SET—based externalist explanations for domestication with a recently formulated alternative developed from niche construction theory (NCT). Archaeological and paleoenvironmental records from two independent centers of domestication in the Americas—eastern North America and the Neotropics of northern South America, are found to support the NCT-based explanatory approach but not the SET explanations, underscoring the limitations of externalist SET approaches and the need for broader conceptualization of the processes that direct evolutionary change in order to gain a better general understanding of initial domestication as well as other major evolutionary transitions.     

Parasites, ecosystems and sustainability: an ecological and complex systems perspective

Host-parasite relationships can be conceptualised either narrowly, where the parasite is metabolically dependent on the host, or more broadly, as suggested by an ecological-evolutionary and complex systems perspective. In this view Host-parasite relationships are part of a larger set of ecological and co-evolutionary interdependencies and a complex adaptive system. These interdependencies affect not just the hosts, vectors, parasites, the immediate agents, but also those indirectly or consequentially affected by the relationship. Host-parasite relationships also can be viewed as systems embedded within larger systems represented by ecological communities and ecosystems. So defined, it can be argued that Host-parasite relationships may often benefit their hosts and contribute significantly to the structuring of ecological communities. The broader, complex adaptive system view also contributes to understanding the phenomenon of disease emergence, the ecological and evolutionary mechanisms involved, and the role of parasitology in research and management of ecosystems in light of the apparently growing problem of emerging infectious diseases in wildlife and humans. An expanded set of principles for integrated parasite management is suggested by this perspective.     

Falcon genomics in the context of conservation,speciation, and human culture

Here, we review the diversity, evolutionary history, and genomics of falcons in the context of their conservation and interactions with humans, and provide a perspective on how new genomic approaches may be applied to expand our knowledge of these topics. For millennia, humans and falcons (genus Falco) have developed unique relationships through falconry, religious rituals, conservation efforts, and human lifestyle transitions. From an evolutionary perspective, falcons remain an enigma. Having experienced several recent radiations, they have reached an unparalleled and almost global distribution, with an intrageneric species richness that is roughly an order of magnitude higher than typical within their family (Falconidae) and across other birds (Phylum: Aves). This diversity has evolved in the context of unusual genomic architecture that includes unique chromosomal rearrangements, relatively low chromosome counts, extremely low microdeletion rates, and high levels of nuclear mitochondrial DNA segments (NUMTs). These genomic peculiarities combine with high levels of ecological and organismal diversity and a legacy of human interactions to make falcons obvious candidates for evolutionary studies, providing unique research opportunities in common topics, including chromosomal evolution, the mechanics of speciation, local adaptation, domestication, and urban adaptation.     

Eco-evolutionary feedbacks drive species interactions

In the biosphere, many species live in close proximity and can thus interact in many different ways. Such interactions are dynamic and fall along a continuum between antagonism and cooperation. Because interspecies interactions are the key to understanding biological communities, it is important to know how species interactions arise and evolve. Here, we show that the feedback between ecological and evolutionary processes has a fundamental role in the emergence and dynamics of species interaction. Using a two-species artificial community, we demonstrate that ecological processes and rapid evolution interact to influence the dynamics of the symbiosis between a eukaryote (Saccharomyces cerevisiae) and a bacterium (Rhizobium etli). The simplicity of our experimental design enables an explicit statement of causality. The niche-constructing activities of the fungus were the key ecological process: it allowed the establishment of a commensal relationship that switched to ammensalism and provided the selective conditions necessary for the adaptive evolution of the bacteria. In this latter state, the bacterial population radiates into more than five genotypes that vary with respect to nutrient transport, metabolic strategies and global regulation. Evolutionary diversification of the bacterial populations has strong effects on the community; the nature of interaction subsequently switches from ammensalism to antagonism where bacteria promote yeast extinction. Our results demonstrate the importance of the evolution-to-ecology pathway in the persistence of interactions and the stability of communities. Thus, eco-evolutionary dynamics have the potential to transform the structure and functioning of ecosystems. Our results suggest that these dynamics should be considered to improve our understanding of beneficial and detrimental host–microbe interactions.     

Neuroendocrine-immune circuits,phenotypes, and interactions

Multidirectional interactions among the immune, endocrine, and nervous systems have been demonstrated in humans and non-human animal models for many decades by the biomedical community, but ecological and evolutionary perspectives are lacking. Neuroendocrine-immune interactions can be conceptualized using a series of feedback loops, which culminate into distinct neuroendocrine-immune phenotypes. Behavior can exert profound influences on these phenotypes, which can in turn reciprocally modulate behavior. For example, the behavioral aspects of reproduction, including courtship, aggression, mate selection and parental behaviors can impinge upon neuroendocrine-immune interactions. One classic example is the immunocompetence handicap hypothesis (ICHH), which proposes that steroid hormones act as mediators of traits important for female choice while suppressing the immune system. Reciprocally, neuroendocrine-immune pathways can promote the development of altered behavioral states, such as sickness behavior. Understanding the energetic signals that mediate neuroendocrine-immune crosstalk is an active area of research. Although the field of psychoneuroimmunology (PNI) has begun to explore this crosstalk from a biomedical standpoint, the neuroendocrine-immune-behavior nexus has been relatively underappreciated in comparative species. The field of ecoimmunology, while traditionally emphasizing the study of non-model systems from an ecological evolutionary perspective, often under natural conditions, has focused less on the physiological mechanisms underlying behavioral responses. This review summarizes neuroendocrine-immune interactions using a comparative framework to understand the ecological and evolutionary forces that shape these complex physiological interactions.     

Social and individual learning of helping in humans and other species

Helping behaviors can be innate, learned by copying others (cultural transmission) or individually learned de novo. These three possibilities are often entangled in debates on the evolution of helping in humans. Here we discuss their similarities and differences, and argue that evolutionary biologists underestimate the role of individual learning in the expression of helping behaviors in humans.     

THE NICHE CONSTRUCTION PERSPECTIVE: A CRITICAL APPRAISAL

Niche construction refers to the activities of organisms that bring about changes in their environments, many of which are evolutionarily and ecologically consequential. Advocates of niche construction theory (NCT) believe that standard evolutionary theory fails to recognize the full importance of niche construction, and consequently propose a novel view of evolution, in which niche construction and its legacy over time (ecological inheritance) are described as evolutionary processes, equivalent in importance to natural selection. Here, we subject NCT to critical evaluation, in the form of a collaboration between one prominent advocate of NCT, and a team of skeptics. We discuss whether niche construction is an evolutionary process, whether NCT obscures or clarifies how natural selection leads to organismal adaptation, and whether niche construction and natural selection are of equivalent explanatory importance. We also consider whether the literature that promotes NCT overstates the significance of niche construction, whether it is internally coherent, and whether it accurately portrays standard evolutionary theory. Our disagreements reflect a wider dispute within evolutionary theory over whether the neo‐Darwinian synthesis is in need of reformulation, as well as different usages of some key terms (e.g., evolutionary process).     

Evaluating the self‐domestication hypothesis of human evolution

“Self‐domestication” has been invoked to understand important aspects of human evolution, integrating physiological, behavioral, and morphological information in a novel way. It proposes that selection for reduced aggression on animals undergoing domestication provides a model for selection favoring prosocial behaviors in humans and for a set of seemingly independent features, which arose as a result of developmental correlation. We review the history of the idea and examine patterns of domestication. A lack of empirical studies on evolutionary rates and variation thwarts meaningful comparison with domestication. The neural crest hypothesis for domestication has great explanatory power but it is difficult to test. We suggest a scenario in which the morphological byproducts of domestication can act as an honest signal of reduced xenophobia. Future studies should test if alternative explanations for the features deemed to result from self‐domestication are mutually exclusive and generate data to test predictions of these hypotheses.     

The phylogenetic component of food web structure and intervality

Despite the exceptional complexity formed by species and their interactions in ecological networks, such as food webs, regularities in the network structures are repeatedly demonstrated. The interactions are determined by the characteristics of a species. The characteristics are in turn determined by the species’ phylogenetic relationships, but also by factors not related to evolutionary history. Here, we test whether species’ phylogenetic relationships provides a significant proxy for food web intervality. We thereafter quantify the degree to which different species traits remain valuable predictors of food web structure after the baseline effect of species’ relatedness has been removed. We find that the phylogenetic relationships provide a significant background from which to estimate food web intervality and thereby structure. However, we also find that there is an important, non-negligible part of some traits, e.g., body size, in food webs that is not accounted for by the phylogenetic relationships. Additionally, both these relationships differ depending if a predator or a prey perspective is adopted. Clearly, species’ evolutionary history as well as traits not determined by phylogenetic relationships shapes predator-prey interactions in food webs, and the underlying evolutionary processes take place on slightly different time scales depending on the direction of predator-prey adaptations.     

The measurement of coevolution in the wild

Coevolution has long been thought to drive the exaggeration of traits, promote major evolutionary transitions such as the evolution of sexual reproduction and influence epidemiological dynamics. Despite coevolution’s long suspected importance, we have yet to develop a quantitative understanding of its strength and prevalence because we lack generally applicable statistical methods that yield numerical estimates for coevolution’s strength and significance in the wild. Here, we develop a novel method that derives maximum likelihood estimates for the strength of direct pairwise coevolution by coupling a well‐established coevolutionary model to spatially structured phenotypic data. Applying our method to two well‐studied interactions reveals evidence for coevolution in both systems. Broad application of this approach has the potential to further resolve long‐standing evolutionary debates such as the role species interactions play in the evolution of sexual reproduction and the organisation of ecological communities.     

Evolutionary Connectionism: Algorithmic Principles Underlying the Evolution of Biological Organisation in Evo-Devo,Evo-Eco and Evolutionary Transitions

The mechanisms of variation, selection and inheritance, on which evolution by natural selection depends, are not fixed over evolutionary time. Current evolutionary biology is increasingly focussed on understanding how the evolution of developmental organisations modifies the distribution of phenotypic variation, the evolution of ecological relationships modifies the selective environment, and the evolution of reproductive relationships modifies the heritability of the evolutionary unit. The major transitions in evolution, in particular, involve radical changes in developmental, ecological and reproductive organisations that instantiate variation, selection and inheritance at a higher level of biological organisation. However, current evolutionary theory is poorly equipped to describe how these organisations change over evolutionary time and especially how that results in adaptive complexes at successive scales of organisation (the key problem is that evolution is self-referential, i.e. the products of evolution change the parameters of the evolutionary process). Here we first reinterpret the central open questions in these domains from a perspective that emphasises the common underlying themes. We then synthesise the findings from a developing body of work that is building a new theoretical approach to these questions by converting well-understood theory and results from models of cognitive learning. Specifically, connectionist models of memory and learning demonstrate how simple incremental mechanisms, adjusting the relationships between individually-simple components, can produce organisations that exhibit complex system-level behaviours and improve the adaptive capabilities of the system. We use the term “evolutionary connectionism” to recognise that, by functionally equivalent processes, natural selection acting on the relationships within and between evolutionary entities can result in organisations that produce complex system-level behaviours in evolutionary systems and modify the adaptive capabilities of natural selection over time. We review the evidence supporting the functional equivalences between the domains of learning and of evolution, and discuss the potential for this to resolve conceptual problems in our understanding of the evolution of developmental, ecological and reproductive organisations and, in particular, the major evolutionary transitions.     

Adaptation and niche construction in human prehistory: a case study from the southern Scandinavian Late Glacial

The niche construction model postulates that human bio-social evolution is composed of three inheritance domains, genetic, cultural and ecological, linked by feedback selection. This paper argues that many kinds of archaeological data can serve as proxies for human niche construction processes, and presents a method for investigating specific niche construction hypotheses. To illustrate this method, the repeated emergence of specialized reindeer (Rangifer tarandus) hunting/herding economies during the Late Palaeolithic (ca 14.7-11.5 kyr BP) in southern Scandinavia is analysed from a niche construction/triple-inheritance perspective. This economic relationship resulted in the eventual domestication of Rangifer. The hypothesis of whether domestication was achieved as early as the Late Palaeolithic, and whether this required the use of domesticated dogs (Canis familiaris) as hunting, herding or transport aids, is tested via a comparative analysis using material culture-based phylogenies and ecological datasets in relation to demographic/genetic proxies. Only weak evidence for sustained niche construction behaviours by prehistoric hunter-gatherer in southern Scandinavia is found, but this study nonetheless provides interesting insights into the likely processes of dog and reindeer domestication, and into processes of adaptation in Late Glacial foragers.     

Ecological and evolutionary consequences of niche construction for its agent

Niche construction can generate ecological and evolutionary feedbacks that have been underinvestigated so far. We present an eco-evolutionary model that incorporates the process of niche construction to reveal its effects on the ecology and evolution of the niche-constructing agent. We consider a simple plant-soil nutrient ecosystem in which plants have the ability to increase the input of inorganic nutrient as an example of positive niche construction. On an ecological time scale, the model shows that niche construction allows the persistence of plants under infertile soil conditions that would otherwise lead to their extinction. This expansion of plants' niche, however, requires a high enough rate of niche construction and a high enough initial plant biomass to fuel the positive ecological feedback between plants and their soil environment. On an evolutionary time scale, we consider that the rates of niche construction and nutrient uptake coevolve in plants while a trade-off constrains their values. Different evolutionary outcomes are possible depending on the shape of the trade-off. We show that niche construction results in an evolutionary feedback between plants and their soil environment such that plants partially regulate soil nutrient content. The direct benefit accruing to plants, however, plays a crucial role in the evolutionary advantage of niche construction.     

Reticulated Origin of Domesticated Emmer Wheat Supports a Dynamic Model for the Emergence of Agriculture in the Fertile Crescent

We used supernetworks with datasets of nuclear gene sequences and novel markers detecting retrotransposon insertions in ribosomal DNA loci to reassess the evolutionary relationships among tetraploid wheats. We show that domesticated emmer has a reticulated genetic ancestry, sharing phylogenetic signals with wild populations from all parts of the wild range. The extent of the genetic reticulation cannot be explained by post-domestication gene flow between cultivated emmer and wild plants, and the phylogenetic relationships among tetraploid wheats are incompatible with simple linear descent of the domesticates from a single wild population. A more parsimonious explanation of the data is that domesticated emmer originates from a hybridized population of different wild lineages. The observed diversity and reticulation patterns indicate that wild emmer evolved in the southern Levant, and that the wild emmer populations in south-eastern Turkey and the Zagros Mountains are relatively recent reticulate descendants of a subset of the Levantine wild populations. Based on our results we propose a new model for the emergence of domesticated emmer. During a pre-domestication period, diverse wild populations were collected from a large area west of the Euphrates and cultivated in mixed stands. Within these cultivated stands, hybridization gave rise to lineages displaying reticulated genealogical relationships with their ancestral populations. Gradual movement of early farmers out of the Levant introduced the pre-domesticated reticulated lineages to the northern and eastern parts of the Fertile Crescent, giving rise to the local wild populations but also facilitating fixation of domestication traits. Our model is consistent with the protracted and dispersed transition to agriculture indicated by the archaeobotanical evidence, and also with previous genetic data affiliating domesticated emmer with the wild populations in southeast Turkey. Unlike other protracted models, we assume that humans played an intuitive role throughout the process.     

Spatial effects favour the evolution of niche construction

We present an individual-based, spatial implementation of an existing two-locus population genetic model of niche construction. Our analysis reveals that, across a broad range of conditions, niche-construction traits can drive themselves to fixation by simultaneously generating selection that favours 'recipient' trait alleles and linkage disequilibrium between niche-construction and recipient trait alleles. The effect of spatiality is key, since it is the local, resource-mediated interaction between recipient and niche-constructing loci which gives rise to gene linkage. Spatial clustering effects point to a possible mechanism by which an initially rare recipient trait whose selection depends on niche construction could establish in an otherwise hostile environment. The same mechanism could also lead to the spread of an established niche-constructing colony. Similar phenomena are observed in the spatial modelling of two species 'engineering webs'. Here, the activities of two niche-constructing species can combine to drive a particular recipient trait to fixation, or in certain circumstances, maintain the presence of polymorphisms through the preservation of otherwise deleterious alleles. This may have some relevance to ecosystem stability and the maintenance of genetic variation, where the frequencies of key resources are affected by the niche-constructing activities of more than one species. Our model suggests that the stability of multi-species webs in natural populations may increase as the complexity of species-environment interactions increases.     

What Do We Study in Evolutionary Ethnobiology? Defining the Theoretical Basis for a Research Program

Many scientific fields investigate the relationship between humans and nature from different perspectives and with a wide range of questions. These fields include, for example, human ecology, human behavioral ecology, and evolutionary psychology, and they are linked through the fact that they all adopt ecological and/or evolutionary hypotheses to understand this phenomenon. In this paper, we define for the first time the field of evolutionary ethnobiology, which seeks to understand these relationships in a broad perspective, considering an interdisciplinary program that integrates the advances, tools, and insights from different scientific fields. This theoretical and methodological integration is necessary for the formation of theoretical bases in ethnobiology and in other areas that investigate the relationship between humans and nature.     

Chimpanzee social intelligence: selfishness,altruism, and the mother–infant bond

To better understand the human mind from an evolutionary perspective, a great deal of research has focused on the closest living relative of humans, the chimpanzee, using various approaches, including studies of social intelligence. Here, I review recent research related to several aspects of social intelligence, including deception, understanding of perception and intention, social learning, trading, cooperation, and regard for others. Many studies have demonstrated that chimpanzees are proficient in using their social intelligence for selfish motives to benefit from their interactions with others. In contrast, it is not yet clear whether chimpanzees engage in prosocial behaviors that benefit others; however, chimpanzee mother–infant interactions indicate the possibility of such behaviors. Therefore, I propose that chimpanzees possess rudimentary traits of human mental competence not only in terms of theory of mind in a broader sense but also in terms of prosociality involving regard for others. Mother–infant interactions appear to be particularly important to understanding the manifestation of social intelligence from an evolutionary perspective.     

The evolution of social behavior in microorganisms

Recent studies of microorganisms have revealed diverse complex social behaviors, including cooperation in foraging, building, reproducing, dispersing and communicating. These microorganisms should provide novel, tractable systems for the analysis of social evolution. The application of evolutionary and ecological theory to understanding their behavior will aid in developing better means to control the many pathogenic bacteria that use social interactions to affect humans.     

The origins of agriculture in the Americas

Three independent centers of domestication and agricultural origin have been identified in the Americas: the south-central Andes, Mexico, and most recently, eastern North America. Much of the evidence for early domesticates in these three regions has been excavated from higher elevation dry caves and rock shelters. These sites contain remarkably well preserved plant and animal remains, along with a record of short-term occupation by small groups of hunter-gatherers and early cultivators. As a result it has long been thought that plants and animals were brought under domestication in the Americas by small, seasonally mobile societies living in upland settings. The age of small seeds and other plant materials recovered from such dry caves and believed to represent early domesticates was, of necessity, determined indirectly, through conventional large-sample radiocarbon dating of organic material thought to be contemporaneous. In each of the three regions, the earliest domesticates were believed to date between 7,000 and 10,000 B.P. The origin of agriculture in the Americas was thought to be roughly contemporary with the transition from foraging to farming in the Near East (Fertile Crescent, ca. 10,000 B.P.) and China (Yangtze Corridor, ca. 8,500 B.P.). Since the mid-1980s, however, the age of many of the proposed early domesticates in the Americas, as well as their contexts of domestication, have been re-examined, beginning in eastern North America. The excavation of larger and more sedentary river valley settlements in eastern North America has yielded ample evidence of the cultivation of domesticated seed plants. This evidence is as old as or older than that recovered from seasonally occupied upland caves and rock shelters. In addition, a new and more rigorous standard for evidence of domestication has been adopted in eastern North America. That standard, which requires direct dating of seeds and other plant parts that exhibit clear, unequivocal, and well-documented morphological markers of domestication, is now being applied throughout the Americas, producing conservative timetables of domestication and agricultural origins that contradict alternative, more speculative chronological frameworks. Under the new standard of evidence, domestication of plants in all three independent centers (and in the Andes, domestication of animals) appears to have taken place between about 5,500 and 4,000 years ago, much more recently than previously was thought. Several lines of evidence also suggest that the Native American societies that first brought these species under domestication may not have been exclusively seasonally mobile hunter-gatherers of higher-elevation environments. In each of the three regions, domesticates recovered from upland caves may reflect a transition to a farming way of life accomplished by societies occupying more sedentary settlements in river valleys. In some cases, upland caves containing domesticates may represent one component in the seasonal round of early food production by societies occupying nearby river valleys; in others, they may mark the subsequent expansion of food production economies out of rich river valley resource zones into adjacent upland environments.     

Native plant/herbivore interactions as determinants of the ecological and evolutionary effects of invasive mammalian herbivores: the case of the common brushtail possum

In their native range, mammalian herbivores exist in a suite of direct and indirect ecological and evolutionary relationships with plant populations and communities. Outside their native range these herbivores become embedded in a multitude of new ecological and evolutionary interactions with native plant species in the new range. Sound knowledge of the plant/herbivore interactions in the herbivores’ native range provides an ideal framework to better understand their effects in the introduced range. The example of the common brushtail possum (Trichosurus vulpecula) and its introduction to New Zealand from Australia provides an excellent case study. In Australia, the common brushtail possum is a widespread generalist herbivore and it is thought that this generalist lifestyle has equipped the species well for successful colonisation of New Zealand. In Australia the brushtail possum has co-existed with highly chemically defended foliage since the Oligocene and recent papers have supported the role of possums as agents of selection on eucalypt defences. While the chemical profile of New Zealand foliage is comparatively poorly understood, possums do show clear selectivity between and within populations and some of these interactions may be mediated by the animals ability to ‘cope’ with PSMs, coupled with maintaining its generalist diet. While possums have had less time to effect evolutionary change in New Zealand species, their impacts on plant fitness have been well documented. However, further knowledge on variation and heritability of foliage traits driving possum preferences is needed to elucidate the ecological and evolutionary plant/possum interactions in the invasive range.