Constructing a familiar, rather uncontroversial comparative psychology framework (cf. Trestman, Reference Trestman2013), Coombs and Trestman assert that selective eco-evolutionary pressures force emergence and development of a phyla-distinct pyramid of complex traits for increasingly recent, sophisticated animal bodies, brains, cognition, and behavior. Pivotal physical and phenomenological traits, particularly active visual sensing, such as visual reafference for monitoring self-action and the visuomotor control of object-oriented actions, are advanced to explain how taxa converge and diverge in their relative evolutionary trajectories into distinct complex-cognition and noncomplex-cognition lineages, with the former now populated by only certain vertebrates, cephalopod mollusks, and euarthropods in the known extant and extinct natural history record. The authors thus characterize complex-cognition lineages by a unique observed set of integrated body, sensory, and motor traits that embody a neural-cognitive “toolkit” for enabling and controlling intricate goal-directed body actions. Some significant multitrait cognitive and behavioral attributions organized into the highest tiers of the authors’ complex-cognition pyramid include central place foraging and unlimited associative learning. While such complex inherited and learned traits are indeed critical for identifying and classifying the expression of complex cognition in animals, specific capabilities for presumed higher-order social interactions have been curiously and frustratingly omitted from Coombs and Trestman’s framework. Experts across many disciplines frequently rate social intelligence and the securing of individual or group cooperation-competition tradeoffs, often falling between extremes of altruistic sacrifice (or moralism and justice) and Machiavellian scheming (or egotism and cheating), as the pinnacle of theory-of-mind drivers and outcomes for cognitive complexity and adaptive behavior (Chen et al., Reference Chen, Martínez and Cheng2018; Clark, Reference Clark2014, Reference Clark2015, Reference Clark2017, Reference Clark2019, Reference Clark2020, Reference Clark2021a,b, Reference Clark2023; de Waal & Preston, Reference de Waal and Preston2017; Dunbar, Reference Dunbar1998; Parker & McKinney, Reference Parker and McKinney1999; Piaget, Reference Piaget1952; Russon et al., Reference Russon, Bard and Parker1996). What is quite instructive, and central to Coombs and Trestman’s thesis, is that the origins and progression of complex cooperative and competitive social traits, such as collective foraging or hunting, cosmopolitan living, abode construction, and mate selection, show remarkable conservation throughout phylogeny, from simpler unicellular to more complicated multicellular life forms invested with or without brains and well-differentiated nervous systems (Clark, Reference Clark2013a, Reference Clark2021c,d). Greater attention to these details may give readers pause in fully accepting the authors’ perhaps too animal-centric trait analysis, rendering new insights about intelligence from crafting a framework with expanded systematics scope.
Comparing complex traits associated with mating across different taxa will help elaborate the evolution of social intelligence and goal-directed behavior. Sex, weakly defined as the exchange and recombination or re-assortment of genetic material during paired reproduction, helps keep harmful mutations from becoming fixed within genomes of isolated populations while perhaps enabling genetic innovations that strengthen selective advantages for progeny and, in instances of horizontal gene transfer of vertically evolved genes, cohorts. Viruses, bacteria, fungi and molds, protozoa, plants, and animals all have evolved sexual or sex-like mechanisms, with increasingly sophisticated eukaryotic cellular life generally depending on isogametes, anisogametes, or oogametes to deploy genomes (Clark, Reference Clark2013a, Reference Clark2021c,d). Mate differentiation, such as different sexes or mating types defined by di- or polymorphisms and other features, represents major evolutionary, ecological, and developmental sociobiological transitions in Earth life that may lead to further transitions. Biased opinions, possibly in agreement with the authors’ own opinions, insist only animals co-evolved the somatic structures (i.e., ornaments and weapons), behavioral routines (e.g., courtship and dominance rituals), and decision-making processes (e.g., learning, memory, and deduction) needed for the sorts of complex sexual selection first described by Darwin and later by founders of the neoDarwinian school of thought (Clark, Reference Clark2013a, Reference Clark2021c,d). These frameworks of sexual selection may be categorically broken into intersexual and intrasexual mechanisms through which social judgments about mate availability, quality or competence, and compatibility can be inferred by courting couples and by rivals. Intersexual selection serves to motivate and coordinate the mating activities of partners in space and time. In contrast, intrasexual selection serves to discourage or prevent successful sexual relations of rival suitors or recipients contending for the same prospective mate(s).
However, phycologists, bacteriologists, and protistologists now recognize that integrated aspects of unicellular microorganism morphology and behavior, more-or-less anecdotally reported by early twentieth-century scientists, fulfill at least some criteria of animal-like mating ornaments and courtship (Clark, Reference Clark2013a, Reference Clark2021c,d). Enterobacteria, yeast, cellular slime molds, and ciliated protozoa, for example, secrete diffusible peptide mating pheromones that motivate intraspecies and sometimes interspecies mates to engage them in either sexual-like monogamous conjugation or other forms of paired reproduction (Clark, Reference Clark2013a, Reference Clark2021c,d). When sensed, gradients of circulating mating pheromones advertise the location and sex or type of mate, automatically inducing an instinctual-like formation of glycoproteins and a conjugation bridge and/or other changes in cell structure with which either both cells fuse and exchange genes or a “male” donor cell physically docks then initiates gene transfer to a “female” recipient cell. For nonmotile microbes, such as some enterococcal bacteria and fungi, pheromone-triggered intraspecies mate selection is a largely random outcome of dynamic ecological conditions favoring cell proximity and contact, where the bridge may serve as ornament or weapon. But microbes, competent at Ca2+-dependent social twitching, flagellar propulsion, ciliary reversals, and additional forms of locomotion amounting to courting dances and dominance displays, show skill at selecting compatible fit mates and at deterring rivals, thus gating the spread of inferior genes due to promiscuous unions. Indeed, this behavior is governed by Hebbian-like learned social logics in ciliated protozoa capable of altruistically or deceptively signaling mating availability and prowess. Contractile ciliates especially demonstrate capacities for planning, searching, and executing learned social strategies, such as switching messages of behavioral propaganda and putatively bestowing beneficial epigenetic “nuptial gifts,” in an effort to minimize survival-reproductive tradeoffs (Clark, Reference Clark2010, Reference Clark2012, Reference Clark2013a,b, Reference Clark2021c,d). Mating decisions reached by these microbes resemble learned social inferences derived from availability and representativeness heuristics of suitor/recipient fitness and correspond to decision-making used by animals experiencing true sexual contexts. Such “cognitive cell” adaptations provide powerful mechanisms for microbes to exploit their environs, enabling niche creation and dominance in previously inhospitable to hospitable eco-evolutionary settings. They also underlie high complexity linked to expression of social intelligence and goal-directed behavior for even primitive life.
Constructing a familiar, rather uncontroversial comparative psychology framework (cf. Trestman, Reference Trestman2013), Coombs and Trestman assert that selective eco-evolutionary pressures force emergence and development of a phyla-distinct pyramid of complex traits for increasingly recent, sophisticated animal bodies, brains, cognition, and behavior. Pivotal physical and phenomenological traits, particularly active visual sensing, such as visual reafference for monitoring self-action and the visuomotor control of object-oriented actions, are advanced to explain how taxa converge and diverge in their relative evolutionary trajectories into distinct complex-cognition and noncomplex-cognition lineages, with the former now populated by only certain vertebrates, cephalopod mollusks, and euarthropods in the known extant and extinct natural history record. The authors thus characterize complex-cognition lineages by a unique observed set of integrated body, sensory, and motor traits that embody a neural-cognitive “toolkit” for enabling and controlling intricate goal-directed body actions. Some significant multitrait cognitive and behavioral attributions organized into the highest tiers of the authors’ complex-cognition pyramid include central place foraging and unlimited associative learning. While such complex inherited and learned traits are indeed critical for identifying and classifying the expression of complex cognition in animals, specific capabilities for presumed higher-order social interactions have been curiously and frustratingly omitted from Coombs and Trestman’s framework. Experts across many disciplines frequently rate social intelligence and the securing of individual or group cooperation-competition tradeoffs, often falling between extremes of altruistic sacrifice (or moralism and justice) and Machiavellian scheming (or egotism and cheating), as the pinnacle of theory-of-mind drivers and outcomes for cognitive complexity and adaptive behavior (Chen et al., Reference Chen, Martínez and Cheng2018; Clark, Reference Clark2014, Reference Clark2015, Reference Clark2017, Reference Clark2019, Reference Clark2020, Reference Clark2021a,b, Reference Clark2023; de Waal & Preston, Reference de Waal and Preston2017; Dunbar, Reference Dunbar1998; Parker & McKinney, Reference Parker and McKinney1999; Piaget, Reference Piaget1952; Russon et al., Reference Russon, Bard and Parker1996). What is quite instructive, and central to Coombs and Trestman’s thesis, is that the origins and progression of complex cooperative and competitive social traits, such as collective foraging or hunting, cosmopolitan living, abode construction, and mate selection, show remarkable conservation throughout phylogeny, from simpler unicellular to more complicated multicellular life forms invested with or without brains and well-differentiated nervous systems (Clark, Reference Clark2013a, Reference Clark2021c,d). Greater attention to these details may give readers pause in fully accepting the authors’ perhaps too animal-centric trait analysis, rendering new insights about intelligence from crafting a framework with expanded systematics scope.
Comparing complex traits associated with mating across different taxa will help elaborate the evolution of social intelligence and goal-directed behavior. Sex, weakly defined as the exchange and recombination or re-assortment of genetic material during paired reproduction, helps keep harmful mutations from becoming fixed within genomes of isolated populations while perhaps enabling genetic innovations that strengthen selective advantages for progeny and, in instances of horizontal gene transfer of vertically evolved genes, cohorts. Viruses, bacteria, fungi and molds, protozoa, plants, and animals all have evolved sexual or sex-like mechanisms, with increasingly sophisticated eukaryotic cellular life generally depending on isogametes, anisogametes, or oogametes to deploy genomes (Clark, Reference Clark2013a, Reference Clark2021c,d). Mate differentiation, such as different sexes or mating types defined by di- or polymorphisms and other features, represents major evolutionary, ecological, and developmental sociobiological transitions in Earth life that may lead to further transitions. Biased opinions, possibly in agreement with the authors’ own opinions, insist only animals co-evolved the somatic structures (i.e., ornaments and weapons), behavioral routines (e.g., courtship and dominance rituals), and decision-making processes (e.g., learning, memory, and deduction) needed for the sorts of complex sexual selection first described by Darwin and later by founders of the neoDarwinian school of thought (Clark, Reference Clark2013a, Reference Clark2021c,d). These frameworks of sexual selection may be categorically broken into intersexual and intrasexual mechanisms through which social judgments about mate availability, quality or competence, and compatibility can be inferred by courting couples and by rivals. Intersexual selection serves to motivate and coordinate the mating activities of partners in space and time. In contrast, intrasexual selection serves to discourage or prevent successful sexual relations of rival suitors or recipients contending for the same prospective mate(s).
However, phycologists, bacteriologists, and protistologists now recognize that integrated aspects of unicellular microorganism morphology and behavior, more-or-less anecdotally reported by early twentieth-century scientists, fulfill at least some criteria of animal-like mating ornaments and courtship (Clark, Reference Clark2013a, Reference Clark2021c,d). Enterobacteria, yeast, cellular slime molds, and ciliated protozoa, for example, secrete diffusible peptide mating pheromones that motivate intraspecies and sometimes interspecies mates to engage them in either sexual-like monogamous conjugation or other forms of paired reproduction (Clark, Reference Clark2013a, Reference Clark2021c,d). When sensed, gradients of circulating mating pheromones advertise the location and sex or type of mate, automatically inducing an instinctual-like formation of glycoproteins and a conjugation bridge and/or other changes in cell structure with which either both cells fuse and exchange genes or a “male” donor cell physically docks then initiates gene transfer to a “female” recipient cell. For nonmotile microbes, such as some enterococcal bacteria and fungi, pheromone-triggered intraspecies mate selection is a largely random outcome of dynamic ecological conditions favoring cell proximity and contact, where the bridge may serve as ornament or weapon. But microbes, competent at Ca2+-dependent social twitching, flagellar propulsion, ciliary reversals, and additional forms of locomotion amounting to courting dances and dominance displays, show skill at selecting compatible fit mates and at deterring rivals, thus gating the spread of inferior genes due to promiscuous unions. Indeed, this behavior is governed by Hebbian-like learned social logics in ciliated protozoa capable of altruistically or deceptively signaling mating availability and prowess. Contractile ciliates especially demonstrate capacities for planning, searching, and executing learned social strategies, such as switching messages of behavioral propaganda and putatively bestowing beneficial epigenetic “nuptial gifts,” in an effort to minimize survival-reproductive tradeoffs (Clark, Reference Clark2010, Reference Clark2012, Reference Clark2013a,b, Reference Clark2021c,d). Mating decisions reached by these microbes resemble learned social inferences derived from availability and representativeness heuristics of suitor/recipient fitness and correspond to decision-making used by animals experiencing true sexual contexts. Such “cognitive cell” adaptations provide powerful mechanisms for microbes to exploit their environs, enabling niche creation and dominance in previously inhospitable to hospitable eco-evolutionary settings. They also underlie high complexity linked to expression of social intelligence and goal-directed behavior for even primitive life.
Financial support
This research received no specific grant from any funding agency, commercial, or not-for-profit sectors.
Competing interests
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