Photo: Daniel Berkowic
Research
General
My research combines theoretical and experimental work and deals with the relationship between Behavior, Ecology and Evolution. While I may be described shortly as a Behavioral Ecologist, I have been also collaborating with psychologists (Ido Erev, Shimon Edelman), mathematicians (Marc Feldman, Uzi Motro, Lewi Stone), and computer scientists (Joe Halpern), in an effort to understand the evolution of learning and decision making mechanisms in humans and animals. My general view of the current challenges in the field is summarized in the goals and scope of the international workshop we organized back in November 2010 (Learning, decision making, and evolutionary theory), and in a short commentary . My ideas about cognitive evolution (see papers with Joe Halpern, Shimon Edelman, and section 2 below) are probably rooted in my early studies on egg and nestling recognition in cuckoo hosts (Lotem 1993, Lotem et al. 1992, 1995), where I first encountered a simple version of the general requirement for co-evolved coordination between learning rules and the timing and the distribution of data input. My past research included studies in cuckoo-host co-evolution, parent-offspring communication and nestling begging, altruism and cooperation, decision making, mate choice, and the evolution of individual and social learning mechanisms.
My research combines theoretical and experimental work and deals with the relationship between Behavior, Ecology and Evolution. While I may be described shortly as a Behavioral Ecologist, I have been also collaborating with psychologists (Ido Erev, Shimon Edelman), mathematicians (Marc Feldman, Uzi Motro, Lewi Stone), and computer scientists (Joe Halpern), in an effort to understand the evolution of learning and decision making mechanisms in humans and animals. My general view of the current challenges in the field is summarized in the goals and scope of the international workshop we organized back in November 2010 (Learning, decision making, and evolutionary theory), and in a short commentary . My ideas about cognitive evolution (see papers with Joe Halpern, Shimon Edelman, and section 2 below) are probably rooted in my early studies on egg and nestling recognition in cuckoo hosts (Lotem 1993, Lotem et al. 1992, 1995), where I first encountered a simple version of the general requirement for co-evolved coordination between learning rules and the timing and the distribution of data input. My past research included studies in cuckoo-host co-evolution, parent-offspring communication and nestling begging, altruism and cooperation, decision making, mate choice, and the evolution of individual and social learning mechanisms.
My current research involves two main projects:
1. From conformity to diversity: Ecological and cognitive determinants of the distribution of learned foraging skills in social groups (Supported by the Israel Science Foundation (2019-2024), with Lucy Aplin).
Recent years have seen increasing interest in research on animal culture and innovation, as well as in studies on social learning - the mechanism through which innovations or new skills are culturally transmitted. An especially debated issue, both theoretically and empirically, has been whether social learning and conformity are always adaptive, and to what extent the tendency to conform suppresses flexibility and diversity. To better tackle this issue, here we propose a new conceptual approach and a research program that views the level of social conformity in a population (along a conformity-diversity spectrum) as strongly affected by ecological factors (such as patch depletion that reduces the profitability of social conformity and favors individual search for alternative patch types), and by task-related cognitive demands that make individual problem solving more difficult than copying or vice-versa. This approach is necessary for teasing apart the effects of ecological and task-specific factors on conformity from variation in the level of conformity that reflects evolved differences in cognitive strategies or in social learning mechanisms.
The current proposal has grown from our attempt to understand the apparent conflict between notable evidence for strong social conformity in animal societies (such as in the study of great tits by Aplin et al., Nature 2015) and our recent findings showing the opposite trend in house sparrows (i.e. individual negative frequency-dependent learning leading to diversity of foraging skills, Aljadeff et. al. 2020). Together with Lucy Aplin we test the hypothesis that a spectrum of outcomes, from social conformity to individual learning based diversity in skill acquisition, can emerge in animal populations (in the house sparrow in this case) depending on experimental conditions that represent different ecological and cognitive demands. First, we will test whether our sparrows can become as conformists as the great tits in Aplin et al.’s study if tested with a similar setup of non-depleted feeders, but still exhibit individual learning based diversity if the same feeders are modified so that food is gradually depleted. Second, we will develop a scale of four learning tasks that differ in the relative difficulty of solution through individual versus social learning. After this scale is established and defined quantitatively (in a set of independent experiments), we will use these four learning tasks, and two conditions of patch depletion, to test the sparrows' tendency to either socially learn and conform or learn alternative solutions a-socially, under the eight possible combinations of ecological and cognitive demands (i.e. to describe their conformity-diversity surface in a 3D phenotypic expression model). Third, the effect of individual variation in idiosyncratic sampling history, and in individual traits (e.g., age, rank, behavioral type, and cognitive performance), on the tendency to conform will be studied by: a) a detailed step-by-step video analysis of individual learning dynamics throughout each experiment, and b) a set of behavioral and cognitive tests of individuals participating in the experiments. The proposed project will thus demonstrate how the combined effects of ecological conditions, task-specific cognitive demands, and individual variation, shape the distribution of social and a-social information in animal populations, and will improve our understanding of what “social learning strategies” really are.
2. Theoretical Models of Cognitive Evolution
(various projects with S. Edelman, J.Y. Halpern, O. Kolodny, M. Arbilly, and R. Bshary)
In the past decade, I have been working with Joe Halpern (Computer Science, Cornell University) on a theoretical model for learning, development, and cognitive evolution (Lotem & Halpern 2008, 2012, Halpern & Lotem 2021). We joined forces with a group of psychologists to present some general cognitive principles for learning structure in time and space (Goldstein et al., 2010, TICS 14: 249-258), and together with Shimon Edelman (Psychology, Cornell) and Oren Kolodny (currently at HUJI), tested these principles using a set of computational simulations in the context of animal learning and creativity (Kolodny et al. 2014, 2015a, 2015b), as well as in the case of human language acquisition (Kolodny et al. 2015, Cog. Sci.). I also used this approach to consider the evolution of cognitive mechanisms in response to cultural innovations (Lotem et al. 2017, PNAS), and for gaining better insight into the evolution of advanced cognition (Arbilly & Lotem 2017, Prat et al. 2021, PLOS Biol.), animal learning (Ben-Oren et al. Animal Cognition in revision), and gene-culture coevolution (Oxford Handbook of Cultural Evolution in review).
My past research includes some of the following projects:
The social dynamics of individual and social learning and the development of individual differences
Supported by the Israel Science Foundation (2015-2019), with Luc-Alain Giraldeau. Univ. of Quebec in Montreal.
see Aljadeff et al. 2020,
Individual decision making in a social context and the evolution of social learning mechanisms: experiments with house sparrows facing risky payoffs
Supported by the Israel Science Foundation (2011-2015)
see Truskanov and Lotem 2015, 2017, Truskanov et al. 2018
Mate choice and the evolution of phenotypic diversity: the unique sexual signals of the East Mediterranean Barn Swallow
Supported by the Israeli Academy of Science and Humanities (2007-2011).
(with R. J. Safran, University of Colorado at Boulder, and Y. Vortman).
see Vorman et al. 2011, 2013, 2015, Safran et al. 2016a, b.
Evolving differences in mate preferences and sexual signals are increasingly recognized as important factors in population divergence and speciation. However, a central question is whether the differences in mating traits among populations are arbitrary or adaptive. This question is especially intriguing when different sexual signals that are used separately by different populations are found to co-exist as multiple signals in a single population of the same species complex. The East Mediterranean Barn Swallow (of the sub-species Hirundo rustica transitiva) provides a unique opportunity to study such a case. Although it is generally similar to other well-studied populations of barn swallows, this population presents an interesting mixture of two traits that are known to be under sexual selection in other populations of this widespread species complex: elongated tail streamers and a dark ventral color which are, separately, signals of male quality in Europe and North America, respectively. Understanding the coexistence of these two traits in the small East Mediterranean population may shed light on the evolutionary processes that caused the differential use of these traits in the large, widespread populations of Europe and North America. In particular, the coexistence of these sexually dimorphic characteristics may be related to the evolution of multiple versus alternative sexual signaling strategies, to the degree of genetic heritability of these traits, and to possible gene flow from other populations.
To explore these hypotheses, we proposed a four-year study of the Israeli population of H. r. transitiva. We tested experimentally whether females prefer either both elongated tail streamers and dark ventral coloration, or only one of these traits. Following Safran et al 2005 (Science 309:2210-12) we use the females' dynamic paternity allocation before and after experimental manipulation of these two male traits, as a powerful method for testing female preferences and its effects on an important currency of evolutionary fitness: paternity. We also examine whether tail length and/or ventral coloration can signal (the same or different) male qualities, such as physiological condition, probability of survival, breeding success, and parental investment (nest building, incubation and food provisioning). The heritability of the two traits is assessed by taking nestlings of known parents to be raised to adulthood in large aviaries at the Tel-Aviv University research zoo, as well as by comparing parent-offspring data from the field (using both in-pair and extra-pair young). To explore the possibility that variation in tail length and ventral coloration can be explained by gene flow from the migratory population of H. r. rustica, we captured individuals from both species in fall and winter roosts and used molecular markers to test whether morphological similarity coincides with genetic similarity. For papers summarizing the results of this project see: Vortamn et al. 2011, 2013, 2015, Dor et al. 2012, Safran et al. 2016a, 2016b).
The evolutionary ecology of social and self learning: theory and experiments in house sparrows
Supported by the US-Israel Bi-National Science Foundation (BSF), 2005-2009.
With Prof. Marcus Feldman (Stanford University), and Prof. Uzi Motro (Hebrew University).
see Katsnelson et al. 2008, 2011a, 2011b, 2014, Arbilly et al. 2010, 2011a, 2011b.
Together with Professor Uzi Motro (Hebrew University) and Professor Marcus W. Feldman (Stanford University), we initiated a research project that combines experimental and theoretical work. We attempt to clarify the genetic, ontogenetic, and behavioral mechanisms of the "searcher-follower" learning tendencies in the house sparrow Passer domesticus; and to explore the theoretical implications of such mechanisms for the evolutionary ecology of social and self learning in animal societies. Using a well established research setup of captive sparrows, we carry out a set of experiments that examine whether hand-raised juveniles can be trained to become "searchers" or "followers" through reinforcement learning (see Katsnelson et al. 2008); and whether individuals that prefer to follow others do poorly in self learning tasks (and vice versa). A cross-fostering experiment will measure the genetic heritability of "searchers" and "followers" tendencies, while a complementary field work will provide additional information on the frequency of these tendencies in natural populations. In light of this research, a rich set of mathematical models and computer simulations will investigate how possible trade-offs between self and social learning may emerge, shape, promote, or suppress the evolution of higher self and social cognitive abilities, and how these trade-offs depend on environmental changes.
Learning in birds and humans: Analysis of learning rules and cognitive biases in a biological system.
Supported by the Israeli Academy of Science and Humanities (2003-2007).
With Prof. Ido Erev, Industrial Engineering and Management, The Technion
Many of the problems I have been studied in relation to the evolution of nestling begging or cuckoo-host coevolution are in fact quite general. My colleague, Professor Ido Erev, a psychologist from the Department of Industrial Engineering and Management at the Technion, Haifa, has been studied somewhat similar problems in human decision making. We have been working together on a project funded by the Israeli Academy of Science and Humanities, through which we combine ideas and experience from our different fields. Both economists and evolutionary biologists attempt to explain behavior in terms of its functionality and rationality, but in both humans and animals, learning mechanisms and cognitive biases may frequently produce sub-optimal behavior and cause clear deviations from maximization. Although most evidence for such deviations comes from human studies, their biological robustness and fitness consequences might well be better studied in a more basic biological system, such as the interaction between bird nestlings and their parents (see below). Our four-year study includes experiments and computer simulations; its object is two-fold: a) To test whether learning by nestlings involves basic forms of deviations from maximization, known from human studies, and to analyze their ecological and evolutionary implications; b) To study how parent-offspring communication remains evolutionarily stable despite the fact that as a result of nestling learning parents may reinforce dishonest or counter-productive begging signals.
Parent-offspring conflict and communication in house sparrow nestlings
Supported by the US-Israel Bi-National Science Foundation (BSF), with Prof. David Winkler, Cornell University.
Motivated by my interest in animal communication, and my previous work on nestling begging (Lotem 1993b, Lotem, Wagner & Balshine-Earn 1999; Lotem 1998a-d), I established a research setup of both captive and free-living house sparrows in order to study nestling begging and parent-offspring communication. The project was initiated in 1995, and was expanded during the years 1996-1999 in collaboration with Professor David Winkler (Cornell University), and with the support of the US-Israel Binational fund (BSF). The first contribution of our begging project was in providing the first experimental evidence for the role of offspring learning in parent-offspring communication (Kedar et al. 2000). The project, as well as my collaboration with Professor Winkler, has continued since then, first through my sabbatical stay at Cornell (2000-2001), and currently in the form of a new chapter in this study (see Lotem & Winkler 2004; Dor et al. 2006; Grodzinski & Lotem 2007; Grodzinski et al. 2008,2009, Dor & Lotem 2009).
The evolution of altruism and cooperation
My work on the evolution of altruism and cooperation includes a study of helping behavior in cooperatively breeding cichlids from Lake Tanganyika (with Dr. Sigal Balshine-Earn, currently at Mcmaster University), and a theoretical work withProf. Lewi Stone, and M. Fishman of Tel-Aviv University. These projects were supported by the Israeli Academy of Science and Humanities during the years 1996-1999, and their derived theoretical work is still ongoing. Our study of helping behavior in cooperatively breeding cichlids showed the existence of space segregation and competition among helpers (Werner et al. 2003). It suggests that such competition may limit the opportunities to provide help, and may be motivated by direct benefits of helping behavior. It also inspired us in developing our idea of signaling components in non-signaling behaviors (Lotem, Wagner & Balshine-Earn 1999), an idea that illustrates how Zahavi's handicap principle can work together with other theories for the evolution of altruism (such as kin selection and reciprocity), and how altruistic behaviors can also evolve as signals of quality or condition.
I formally tested some of these ideas together with L. Stone and M. Fishman. Using computer simulations and game theory, we found that, in heterogeneous populations, the tendency to help should be conditioned upon individual quality (i.e. help only when you can afford the cost of helping). This phenomenon is crucial for the evolutionary stability of cooperation (via direct and indirect reciprocity) because as a result of defection by poor phenotypes, discriminative altruism by high-quality individuals becomes the dominating stable strategy (Lotem et al. 1999, Nature 400:226-227; Fishman et al. 2001). Furthermore, we have recently shown that as a result of the emergent correlation between cooperation and individual quality in reciprocity games, signaling benefits of altruistic acts (i.e. quality advertisement) can establish a stable generosity by high quality individuals that no longer depends on the probability of future reciprocation or punishment (Lotem et al. 2003).
Mate choice and mating strategies
In addition to our recent barn swallows project (see above) I have been also involved in the study of mate choice and mating behavior through some theoretical work (Fishman et al. 2003), and as part of my work with my Student, Noam Werner, who studied mate choice in the haplochromine cichlid fish Astatotilapia flaviijosephi. Our study provides the first experimental evidence for male mate choice in a lekking species (Werner & Lotem 2003), and for sequential male mate preference in this species that strongly suggests a trade-off between present and future reproductive effort (Werner & Lotem, 2006). Considering the intense competition among lekking males, our work also suggests that male choosiness may help to solve the so called 'paradox of the lek'. This is because it can make less attractive females more available to subordinate males, thereby increasing the contribution of the latter to the population gene pool and keeping genetic variability among males at a level that justifies female choice.
