The evolution of social philopatry in female primates.

The transition from solitary life to sociality is considered one of the major transitions in evolution. In primates, this transition is currently not well understood. Traditional verbal models appear insufficient to unravel the complex interplay of environmental and demographic factors involved in the evolution of primate sociality, and recent phylogenetic reconstructions have produced conflicting results. We therefore analyze a theoretical model for the evolution of female social philopatry that sheds new light on the question why most primates live in groups. In individual-based simulations, we study the evolution of dispersal strategies of both resident females and their offspring. The model reveals that social philopatry can evolve through kin selection, even if retention of offspring is costly in terms of within-group resource competition and provides no direct benefits. Our model supports the role of predator avoidance as a selective pressure for group-living in primates, but it also suggests that a second benefit of group-living, communal resource defense, might be required to trigger the evolution of sizable groups. Lastly, our model reveals that seemingly small differences in demographic parameters can have profound effects on primate social evolution.

Reproductive tolerance in male primates: Old paradigms and new evidence.

Within social groups of primates, males commonly compete over reproduction, but they may also rely on cooperation with other males. Theory suggests that it may be adaptive for male primates to tolerate some reproduction by other males if reproductive tolerance fosters cooperation, particularly that dominant males yield so-called reproductive concessions to subordinates to entice their cooperation. We review four recent studies that claimed to have found evidence for reproductive concessions or similar forms of reproductive tolerance. However, upon critical reevaluation of their results, no study provides conclusive support for reproductive concessions as predicted by theoretical models. Yet two studies demonstrated a form of reproductive tolerance that cannot be explained by any of the existing models, and that seems to have evolved only in multi-male, multi-female societies with diverse strategic options for males. Our article provides guidance how to study this form of reproductive tolerance in the absence of a unifying model.

From Individual to Group Territoriality: Competitive Environments Promote the Evolution of Sociality.

In many animal species individuals compete for the sole possession of a breeding territory, whereas in other species communal territories are shared among same-sex conspecifics. Under what conditions does natural selection favor the evolution of individual territoriality, and under what conditions does it favor the evolution of sociality? We develop a self-consistent game-theoretic model that allows for feedbacks between evolutionary and population dynamics. In this model, nonresident floaters can chose between three strategies: they can wait for a territory vacancy to arise, they can try to forcefully take over an already-occupied territory, or they can share a territory with an established resident. We show that competitive environments initially favor the evolution of an aggressive (territorial) strategy. Yet as competition increases further, a shift occurs from aggressive to social strategies. Moreover, territory owners (residents) respond to the behavior of floaters, such that a feedback occurs in which residents adjust their degree of tolerance to the level of floater aggression and vice versa. This feedback resembles the dynamics of a biological market and eventually leads to the coexistence of aggressive and social floater strategies in the population. Such mixed equilibria commonly occur in nature.

Transparency, usability, and reproducibility: Guiding principles for improving comparative databases using primates as examples.

Recent decades have seen rapid development of new analytical methods to investigate patterns of interspecific variation. Yet these cutting-edge statistical analyses often rely on data of questionable origin, varying accuracy, and weak comparability, which seem to have reduced the reproducibility of studies. It is time to improve the transparency of comparative data while also making these improved data more widely available. We, the authors, met to discuss how transparency, usability, and reproducibility of comparative data can best be achieved. We propose four guiding principles: 1) data identification with explicit operational definitions and complete descriptions of methods; 2) inclusion of metadata that capture key characteristics of the data, such as sample size, geographic coordinates, and nutrient availability (for example, captive versus wild animals); 3) documentation of the original reference for each datum; and 4) facilitation of effective interactions with the data via user friendly and transparent interfaces. We urge reviewers, editors, publishers, database developers and users, funding agencies, researchers publishing their primary data, and those performing comparative analyses to embrace these standards to increase the transparency, usability, and reproducibility of comparative studies.

Longevity suppresses conflict in animal societies.

Models of social conflict in animal societies generally assume that within-group conflict reduces the value of a communal resource. For many animals, however, the primary cost of conflict is increased mortality. We develop a simple inclusive fitness model of social conflict that takes this cost into account. We show that longevity substantially reduces the level of within-group conflict, which can lead to the evolution of peaceful animal societies if relatedness among group members is high. By contrast, peaceful outcomes are never possible in models where the primary cost of social conflict is resource depletion. Incorporating mortality costs into models of social conflict can explain why many animal societies are so remarkably peaceful despite great potential for conflict.

Facing the crowd: intruder pressure, within-group competition, and the resolution of conflicts over group-membership.

Recent theory in social evolution has been mainly concerned with competition and cooperation within social groups of animals and their impact on the stability of those groups. Much less attention has been paid to conflicts arising as a result of solitary floaters (outsiders) attempting to join groups of established residents (insiders). We model such conflicts over group-membership using a demographically explicit approach in which the rates of births and deaths in a population determine the availability of group-vacancies and the number of floaters competing over these vacancies. We find that the outcome of within-group competition, reflected in the partitioning of reproduction among group members, exerts surprisingly little influence on the resolution of insider-outsider conflict. The outcome of such conflict is also largely unaffected by differences in resource holding potential between insiders and outsiders. By contrast, whether or not groups form is mainly determined by demographic factors (variation in vital rates such as fecundity and mortality) and the resulting population dynamics. In particular, at high floater densities territory defense becomes too costly, and groups form because insiders give in to the intruder pressure imposed on them by outsiders. We emphasize the importance of insider-outsider conflicts in social evolution theory and highlight avenues for future research.

Communal defense of territories and the evolution of sociality.

The evolution of group living has attracted considerable attention from behavioral ecologists working on a wide range of study species. However, theoretical research in this field has been largely focused on cooperative breeders. We extend this line of work to species that lack alloparental care (hereafter termed "noncooperative species") but that may benefit from grouping by jointly defending a common territory. We adopt a demographically explicit approach in which the rates of births and deaths as well as the dispersal decisions of individuals in the population determine the turnover rates of territories and the competition for breeding vacancies thus arising. Our results reveal that some of the factors thought to affect the evolution of cooperative breeding also affect the evolution of group living in noncooperative species. Specifically, high fecundity and low mortality of resident individuals both increase the degree of habitat saturation and make joining an established group more profitable for nonresidents (floaters). Moreover, if floaters can forcefully take over territories, the degree of habitat saturation also affects the chance that residents become targets of takeovers. In this situation, communal defense of territories becomes an important benefit that further promotes the evolution of group living.

Costs and benefits of multi-male associations in redfronted lemurs (Eulemur fulvus rufus).

The evolution of group-living has fascinated but also puzzled researchers from the inception of behavioural ecology. We use a simple optimality approach to examine some of the costs and benefits of group-living in redfronted lemurs (Eulemur fulvus rufus). We show that dominant males profit from accepting subordinates within their groups, as the latter significantly decrease the likelihood that the group is taken over by intruders. This benefit is large enough to outweigh the costs of reproductive competition and may constitute the driving force behind the evolution of multi-male associations in this species.

Even adult sex ratios in lemurs: Potential costs and benefits of subordinate males in Verreaux's sifaka (Propithecus verreauxi) in the Kirindy Forest CFPF, Madagascar.

Optimal group size and composition are determined by both the costs and benefits of group living for the group's members. Verreaux's sifakas (Propithecus verreauxi), a diurnal lemur, form multimale multifemale groups with the tendency toward even adult sex ratios despite a small average number of females per group. The unexpected presence of multiple adult males may be explained by tolerance of other group members if subordinate males provide benefits to the group that outweigh the costs associated with their presence. Results based on both demographic data collected over a 13-year period and behavioral observations suggest that subordinate males provide no benefits in terms of infant survival and defense against group takeover by outside males. Although groups with more males are more likely to win intergroup encounters, subordinate males do not participate in these encounters more often than expected. Subordinate males are not costly to other group members in terms of direct intragroup feeding competition, but aggression rates between dominant and immigrated subordinate males increase in the mating season. Even though subordinate males provide very few benefits to the group, they are not very costly either and thus may be tolerated by resident females and dominant males. This tolerance may help to partially explain the tendency towards their unusual adult sex ratio.

Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors.

Compared to the overall multiplicity of more than 20 plant Hsfs, detailed analyses are mainly restricted to tomato and Arabidopsis and to three important representatives of the family (Hsfs A1, A2 and B1). The three Hsfs represent examples of striking functional diversification specialized for the three phases of the heat stress (hs) response (triggering, maintenance and recovery). This is best illustrated for the tomato Hsf system: (i) HsfA1a is the master regulator responsible for hs-induced gene expression including synthesis of HsfA2 and HsfB1. It is indispensible for the development of thermotolerance. (ii) Although functionally equivalent to HsfA1a, HsfA2 is exclusively found after hs induction and represents the dominant Hsf, the "working horse" of the hs response in plants subjected to repeated cycles of hs and recovery in a hot summer period. Tomato HsfA2 is tightly integrated into a network of interacting proteins (HsfA1a, Hsp17-CII, Hsp17-CI) influencing its activity and intracellular distribution. (iii) Because of structural peculiarities, HsfB1 acts as coregulator enhancing the activity of HsfA1a and/or HsfA2. But in addition, it cooperates with yet to be identified other transcription factors in maintaining and/or restoring housekeeping gene expression.

Role of Hsp17.4-CII as coregulator and cytoplasmic retention factor of tomato heat stress transcription factor HsfA2.

HsfA2 is a heat stress (hs)-induced Hsf in peruvian tomato (Lycopersicon peruvianum) and the cultivated form Lycopersicon esculentum. Due to the high activator potential and the continued accumulation during repeated cycles of heat stress and recovery, HsfA2 becomes a dominant Hsf in thermotolerant cells. The formation of heterooligomeric complexes with HsfA1 leads to nuclear retention and enhanced transcriptional activity of HsfA2. This effect seems to represent one part of potential molecular mechanisms involved in its activity control. As shown in this paper, the activity of HsfA2 is also controlled by a network of nucleocytoplasmic small Hsps influencing its solubility, intracellular localization and activator function. By yeast two-hybrid interaction and transient coexpression studies in tobacco (Nicotiana plumbaginifolia) mesophyll protoplasts, we found that tomato (Lycopersicon esculentum) Hsp17.4-CII acts as corepressor of HsfA2. Given appropriate conditions, both proteins together formed large cytosolic aggregates which could be solubilized in presence of class CI sHsps. However, independent of the formation of aggregates or of the nucleocytoplasmic distribution of HsfA2, its transcriptional activity was specifically repressed by interaction of Hsp17.4-CII with the C-terminal activator domain. Although not identical in all aspects, the situation with the highly expressed, heat stress-inducible Arabidopsis HsfA2 was found to be principally similar. In corresponding reporter assays its activity was repressed in presence of AtHsp17.7-CII but not of AtHsp17.6-CII or LpHsp17.4-CII.

Characterization of C-terminal domains of Arabidopsis heat stress transcription factors (Hsfs) and identification of a new signature combination of plant class A Hsfs with AHA and NES motifs essential for activator function and intracellular localization.

Heat stress transcription factors (Hsfs) are the major regulators of the plant heat stress (hs) response. Sequencing of the Arabidopsis genome revealed the existence of 21 open-reading frames (ORFs) encoding putative Hsfs assigned to classes A-C. Here we present results of a functional genomics approach to the Arabidopsis Hsf family focused on the analysis of their C-terminal domains (CTDs) harboring conserved modules for their function as transcription factors and their intracellular localization. Using reporter assays in tobacco protoplasts and yeast as well as glutathione-S-transferase (GST) pull-down assays, we demonstrate that short peptide motifs enriched with aromatic and large hydrophobic amino acid (aa) residues embedded in an acidic surrounding (AHA motifs) are essential for transcriptional activity of class A Hsfs. In contrast to this, class B and C Hsfs lack AHA motifs and have no activator function on their own. We also provide evidence for the function of a leucine (Leu)-rich region centered around a conserved QMGPhiL motif at the very C-terminus as a nuclear export signal (NES) of class A Hsfs. Sequence comparison indicates that the combination of a C-terminal AHA motif with the consensus sequence FWxxF/L,F/I/L as well as the adjacent NES represents a signature domain for plant class A Hsfs, which allowed to identify more than 60 new Hsfs from the expressed sequence tag (EST) database.

Tomato heat stress protein Hsp16.1-CIII represents a member of a new class of nucleocytoplasmic small heat stress proteins in plants.

We describe a new class of plant small heat stress proteins (sHsps) with dominant nuclear localization (Hsp17-CIII). The corresponding proteins in tomato, Arabidopsis, and rice are encoded by unique genes containing a short intron in the beta4-encoding region of the alpha-crystallin domain (ACD). The strong nuclear localization results from a cluster of basic amino acid residues in the loop between beta5 and beta6 of the ACD. Using yeast 2-hybrid tests, analyses of native complexes of the sHsps, and immunofluorescence data, we demonstrate that, in contrast to earlier observations (Kirschner et al 2000), proteins of the sHsp classes CI, CII, and CIII interact with each other, thereby influencing oligomerization state and intracellular localization.