scholarly journals Isotocin neuronal phenotypes differ among social systems in cichlid fishes

2017 ◽  
Vol 4 (5) ◽  
pp. 170350 ◽  
Author(s):  
Adam R. Reddon ◽  
Constance M. O'Connor ◽  
Erin Nesjan ◽  
Jason Cameron ◽  
Jennifer K. Hellmann ◽  
...  

Social living has evolved numerous times across a diverse array of animal taxa. An open question is how the transition to a social lifestyle has shaped, and been shaped by, the underlying neurohormonal machinery of social behaviour. The nonapeptide neurohormones, implicated in the regulation of social behaviours, are prime candidates for the neuroendocrine substrates of social evolution. Here, we examined the brains of eight cichlid fish species with divergent social systems, comparing the number and size of preoptic neurons that express the nonapeptides isotocin and vasotocin. While controlling for the influence of phylogeny and body size, we found that the highly social cooperatively breeding species ( n  = 4) had fewer parvocellular isotocin neurons than the less social independently breeding species ( n  = 4), suggesting that the evolutionary transition to group living and cooperative breeding was associated with a reduction in the number of these neurons. In a complementary analysis, we found that the size and number of isotocin neurons significantly differentiated the cooperatively breeding from the independently breeding species. Our results suggest that isotocin is related to sociality in cichlids and may provide a mechanistic substrate for the evolution of sociality.

2017 ◽  
Vol 4 (3) ◽  
pp. 160891 ◽  
Author(s):  
Shagun Jindal ◽  
Aneesh P. H. Bose ◽  
Constance M. O'Connor ◽  
Sigal Balshine

Infanticide and offspring cannibalism are taxonomically widespread phenomena. In some group-living species, a new dominant individual taking over a group can benefit from infanticide if doing so induces potential mates to become reproductively available sooner. Despite widespread observations of infanticide (i.e. egg cannibalism) among fishes, no study has investigated whether egg cannibalism occurs in fishes as a result of group takeovers, or how this type of cannibalism might be adaptive. Using the cooperatively breeding cichlid, Neolamprologus pulcher , we tested whether new unrelated males entering the dominant position in a social group were more likely to cannibalize eggs, and whether such cannibalism would shorten the interval until the female's next spawning. Females spawned again sooner if their broods were removed than if they were cared for. Egg cannibalism occurred frequently after a group takeover event, and was rarer if the original male remained with the group. While dominant breeder females were initially highly aggressive towards newcomer males that took over the group, the degree of resistance depended on relative body size differences between the new pair and, ultimately, female aggression did not prevent egg cannibalism. Egg cannibalism, however, did not shorten the duration until subsequent spawning, or increase fecundity during subsequent breeding in our laboratory setting. Our results show that infanticide as mediated through group takeovers is a taxonomically widespread behaviour.


Behaviour ◽  
2014 ◽  
Vol 151 (1) ◽  
pp. 47-71 ◽  
Author(s):  
Kristina Hick ◽  
Adam R. Reddon ◽  
Constance M. O’Connor ◽  
Sigal Balshine

The costs and benefits of engaging in a contest will differ depending on the social situation of the individuals involved. Therefore, understanding contest behaviour can help to elucidate the trade-offs of living in differing social systems and shed light on the evolution of social behaviour. In the current study, we compared contest behaviour in two closely related species of Lamprologine cichlid fish. Neolamprologus pulcher and Telmatochromis temporalis are both pair-breeding cichlids, but N. pulcher are highly social, group-living fish, while T. temporalis display no grouping behaviour. To examine how competition varies by species, sex and familiarity, we staged same-sex conspecific contests over a shelter, a resource that is highly valued by both species, where contestants were either familiar or unfamiliar to one another. When we examined tactical and strategic components of these contests, we found that the highly social species had shorter contests and engaged in fewer costly aggressive acts than did the non-social species. Individuals of the highly social species were also more likely to resolve conflicts through the use of submissive displays, while individuals of the non-social species were more likely to flee from conflict. Familiarity increased the use of submissive displays in the highly social species but not in the less social species. Our findings suggest that conflict resolution behaviour and dominance hierarchy formation are fundamentally linked to the evolution of complex social systems.


2014 ◽  
Vol 369 (1642) ◽  
pp. 20130361 ◽  
Author(s):  
Geoff Wild ◽  
Cody Koykka

In cooperatively breeding species, individuals help to raise offspring that are not their own. We use two inclusive-fitness models to study the advantage of this kind of helpful behaviour in social groups with high reproductive skew. Our first model does not allow for competition among relatives to occur but our second model does. Specifically, our second model assumes a competitive hierarchy among nest-mates, with non-breeding helpers ranked higher than their newborn siblings. For each model, we obtain an expression for the change in inclusive fitness experienced by a helpful individual in a selfish population. The prediction suggested by each expression is confirmed with computer simulation. When model predictions are compared to one another, we find that helping emerges under a broader range of conditions in the second model. Although competition among kin occurs in our second model, we conclude that the life-history features associated with this competition also act to promote the evolutionary transition from solitary to cooperative breeding.


Behaviour ◽  
2015 ◽  
Vol 152 (12-13) ◽  
pp. 1821-1839 ◽  
Author(s):  
Isaac Y. Ligocki ◽  
Adam R. Reddon ◽  
Jennifer K. Hellmann ◽  
Constance M. O’Connor ◽  
Susan Marsh-Rollo ◽  
...  

In group living animals, individuals may visit other groups. The costs and benefits of such visits for the members of a group will depend on the attributes and intentions of the visitor, and the social status of responding group members. Using wild groups of the cooperatively breeding cichlid fish (Neolamprologus pulcher), we compared group member responses to unfamiliar ‘visiting’ conspecifics in control groups and in experimentally manipulated groups from which a subordinate the same size and sex as the visitor was removed. High-ranking fish were less aggressive towards visitors in removal groups than in control groups; low-ranking subordinates were more aggressive in the removal treatment. High-ranking females and subordinates the same size and sex as the visitor responded most aggressively toward the visitor in control groups. These results suggest that visitors are perceived as potential group joiners, and that such visits impose different costs and benefits on current group members.


2022 ◽  
Author(s):  
Allison E. Johnson ◽  
Joseph F. Welklin ◽  
Ian R. Hoppe ◽  
Daizaburo Shizuka

Cooperatively breeding species exhibit a range of social behaviors associated with different costs and benefits to group-living, often in association with different environmental conditions. For example, species in which collective-care of offspring reduces the cost of reproduction are more common in harsh environments (true cooperative breeding), while species that collectively defend resources are present in benign environments (family-living). Here, we examine whether environment also shapes sociality within cooperatively-breeding species. We illustrate that Purple-backed Fairywrens, which primarily gain intrinsic, or collective-care benefits, have larger groups in hot, dry environments and smaller groups in cool, wet environments, whereas Superb Fairywrens which primarily gain extrinsic, or resource defense benefits, exhibit the opposite trend. We suggest differences in the costs and benefits of sociality contribute to these opposing ecogeographic patterns, demonstrating that comparisons of intraspecific patterns of social variation across species can provide insight into how ecology shapes transitions between social systems.


2010 ◽  
Vol 88 (3) ◽  
pp. 334-346 ◽  
Author(s):  
Maxence Salomon ◽  
Samantha Vibert ◽  
Robert G. Bennett

Animal social systems come in a wide range of forms characterized by different types of group-living relationships. Species that express facultative group-living behaviours, where individuals only associate under certain conditions or at certain times, are especially interesting for studying social evolution. We investigated the social structure of the western black widow spider ( Latrodectus hesperus Chamberlin and Ivie, 1935) over 5 years in a coastal British Columbia habitat, and present the first comprehensive evidence of facultative group living in the genus Latrodectus Walckenaer, 1805. Latrodectus hesperus have a flexible social structure that varies seasonally, wherein individuals (mostly females) either form groups or live solitarily. In the fall and early winter, females spontaneously form groups of 2–8 individuals, but live alone during the oviposition season in the spring and summer. When living in groups spiders share large webs and are tolerant of each other, although they appear to forage individually. We also report on the relationships between different ecological factors and the social structure of L. hesperus, including the interaction of these spiders with two co-occurring species of introduced spiders ( Tegenaria agrestis (Walckenaer, 1802) and Tegenaria duellica Simon, 1875). Our findings suggest that L. hesperus is a good model system with which to explore the mechanisms involved in the evolution of sociality.


2016 ◽  
Vol 113 (15) ◽  
pp. 4104-4109 ◽  
Author(s):  
Frank Groenewoud ◽  
Joachim Gerhard Frommen ◽  
Dario Josi ◽  
Hirokazu Tanaka ◽  
Arne Jungwirth ◽  
...  

Predation risk is a major ecological factor selecting for group living. It is largely ignored, however, as an evolutionary driver of social complexity and cooperative breeding, which is attributed mainly to a combination of habitat saturation and enhanced relatedness levels. Social cichlids neither suffer from habitat saturation, nor are their groups composed primarily of relatives. This demands alternative ecological explanations for the evolution of advanced social organization. To address this question, we compared the ecology of eight populations of Neolamprologus pulcher, a cichlid fish arguably representing the pinnacle of social evolution in poikilothermic vertebrates. Results show that variation in social organization and behavior of these fish is primarily explained by predation risk and related ecological factors. Remarkably, ecology affects group structure more strongly than group size, with predation inversely affecting small and large group members. High predation and shelter limitation leads to groups containing few small but many large members, which is an effect enhanced at low population densities. Apparently, enhanced safety from predators by cooperative defense and shelter construction are the primary benefits of sociality. This finding suggests that predation risk can be fundamental for the transition toward complex social organization, which is generally undervalued.


2015 ◽  
Vol 2 (2) ◽  
pp. 140072 ◽  
Author(s):  
Adam R. Reddon ◽  
Constance M. O'Connor ◽  
Susan E. Marsh-Rollo ◽  
Sigal Balshine ◽  
Magdalena Gozdowska ◽  
...  

The mammalian nonapeptide hormones, vasopressin and oxytocin, are known to be potent regulators of social behaviour. Teleost fishes possess vasopressin and oxytocin homologues known as arginine vasotocin (AVT) and isotocin (IT), respectively. The role of these homologous nonapeptides in mediating social behaviour in fishes has received far less attention. The extraordinarily large number of teleost fish species and the impressive diversity of their social systems provide us with a rich test bed for investigating the role of nonapeptides in regulating social behaviour. Existing studies, mostly focused on AVT, have revealed relationships between the nonapeptides, and both social behaviour and dominance status in fishes. To date, much of the work on endogenous nonapeptides in fish brains has measured genomic or neuroanatomical proxies of nonapeptide production rather than the levels of these molecules in the brain. In this study, we measure biologically available AVT and IT levels in the brains of Neolamprologus pulcher , a cooperatively breeding cichlid fish, using high performance liquid chromatography with fluorescence detection. We found that brain AVT levels were higher in the subordinate than in dominant animals, and levels of IT correlated negatively with the expression of affiliative behaviour. We contrast these results with previous studies, and we discuss the role the nonapeptide hormones may play in the regulation of social behaviour in this highly social animal.


2016 ◽  
Vol 94 (5) ◽  
pp. 373-378 ◽  
Author(s):  
Adam R. Reddon ◽  
Constance M. O’Connor ◽  
Isaac Y. Ligocki ◽  
Jennifer K. Hellmann ◽  
Susan E. Marsh-Rollo ◽  
...  

The social brain hypothesis posits that frequent social interactions, characteristic of group living species, select for greater socio-cognitive abilities and the requisite neural machinery. An extension of the social brains hypothesis, known as the cooperative breeding brain hypothesis, postulates that cooperatively breeding species, which live in stable social groups and provide allocare, face particularly pronounced cognitive demands because they must recognize, remember, and differentially respond to multiple group members. These socio-cognitive challenges are thought to have selected for increased cognitive capacity, supported by a bigger brain. To test the prediction that cooperative breeders have larger brains, we performed a phylogenetically controlled comparison of the whole brain masses of adult fish from 16 closely related species of cooperatively and independently breeding lamprologine cichlid species from Lake Tanganyika. We collected data on brain mass from males of eight species of lamprologine cichlids and added this to brain mass data from eight more species found in the published literature. Controlling for body size and phylogeny, we found that cooperative breeding species did not have larger brains, and this was true of for both our field-collected data set and the expanded data set including published values. This study adds to a growing body of literature from other taxa that cast doubt on the cooperative breeding brain hypothesis.


2013 ◽  
Vol 280 (1772) ◽  
pp. 20132245 ◽  
Author(s):  
Christina Riehl

Cooperatively breeding animals live in social groups in which some individuals help to raise the offspring of others, often at the expense of their own reproduction. Kin selection—when individuals increase their inclusive fitness by aiding genetic relatives—is a powerful explanation for the evolution of cooperative breeding, particularly because most groups consist of family members. However, recent molecular studies have revealed that many cooperative groups also contain unrelated immigrants, and the processes responsible for the formation and maintenance of non-kin coalitions are receiving increasing attention. Here, I provide the first systematic review of group structure for all 213 species of cooperatively breeding birds for which data are available. Although the majority of species (55%) nest in nuclear family groups, cooperative breeding by unrelated individuals is more common than previously recognized: 30% nest in mixed groups of relatives and non-relatives, and 15% nest primarily with non-relatives. Obligate cooperative breeders are far more likely to breed with non-kin than are facultative cooperators, indicating that when constraints on independent breeding are sufficiently severe, the direct benefits of group membership can substitute for potential kin-selected benefits. I review three patterns of dispersal that give rise to social groups with low genetic relatedness, and I discuss the selective pressures that favour the formation of such groups. Although kin selection has undoubtedly been crucial to the origin of most avian social systems, direct benefits have subsequently come to play a predominant role in some societies, allowing cooperation to persist despite low genetic relatedness.


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