scholarly journals The brood parasite's guide to inclusive fitness theory

2019 ◽  
Vol 374 (1769) ◽  
pp. 20180198 ◽  
Author(s):  
Ros Gloag ◽  
Madeleine Beekman

Hamilton's theory of inclusive fitness provides a framework for understanding the evolution of social behaviour between kin, including parental and alloparental care. Brood parasitism is a reproductive tactic in which parasites exploit the care of other individuals of the same species (conspecific parasitism) or different species (interspecific parasitism) to rear their brood. Here, drawing from examples in birds and social insects, we identify two insights into brood parasitism that stem from inclusive fitness theory. First, the kin structure within nests, or between neighbouring nests, can create a niche space favouring the evolution of conspecific parasitism. For example, low average relatedness within social insect nests can increase selection for reproductive cheats. Likewise, high average relatedness between adjacent nests of some birds can increase a female's tolerance of parasitism by her neighbour. Second, intrabrood conflict will be high in parasitized broods, from the perspective of both parasite and host young, relative to unparasitized broods. We also discuss offspring recognition by hosts as an example of discrimination in a kin-selected social behaviour. We conclude that the inclusive fitness framework is instructive for understanding aspects of brood parasite and host evolution. In turn, brood parasites present some unique opportunities to test the predictions of inclusive fitness theory.This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.

Author(s):  
Samir Okasha

Inclusive fitness theory, originally due to W. D. Hamilton, is a popular approach to the study of social evolution, but shrouded in controversy. The theory contains two distinct aspects: Hamilton’s rule (rB > C); and the idea that individuals will behave as if trying to maximize their inclusive fitness in social encounters. These two aspects of the theory are logically separable but often run together. A generalized version of Hamilton’s rule can be formulated that is always true, though whether it is causally meaningful is debatable. However, the individual maximization claim only holds true if the payoffs from the social encounter are additive. The notion that inclusive fitness is the ‘goal’ of individuals’ social behaviour is less robust than some of its advocates acknowledge.


2019 ◽  
Vol 374 (1769) ◽  
pp. 20180203 ◽  
Author(s):  
Jukka Suhonen ◽  
Jaakko J. Ilvonen ◽  
Tommi Nyman ◽  
Jouni Sorvari

Interspecific brood parasitism is common in many animal systems. Brood parasites enter the nests of other species and divert host resources for producing their own offspring, which can lead to strong antagonistic parasite–host coevolution. Here, we look at commonalities among social insect species that are victims of brood parasites, and use phylogenetic data and information on geographical range size to predict which species are most probably to fall victims to brood parasites in the future. In our analyses, we focus on three eusocial hymenopteran groups and their brood parasites: (i) bumblebees, (ii) Myrmica ants, and (iii) vespine and polistine wasps. In these groups, some, but not all, species are parasitized by obligate workerless inquilines that only produce reproductive-caste descendants. We find phylogenetic signals for geographical range size and the presence of parasites in bumblebees, but not in ants and wasps. Phylogenetic logistic regressions indicate that the probability of being attacked by one or more brood parasite species increases with the size of the geographical range in bumblebees, but the effect is statistically only marginally significant in ants. However, non-phylogenetic logistic regressions suggest that bumblebee species with the largest geographical range sizes may have a lower likelihood of harbouring social parasites than do hosts with medium-sized ranges. Our results provide new insights into the ecology and evolution of host–social parasite systems, and indicate that host phylogeny and geographical range size can be used to predict threats posed by social parasites, as well to design efficient conservation measures for both hosts and their parasites. This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.


2014 ◽  
Vol 369 (1642) ◽  
pp. 20130565 ◽  
Author(s):  
Ben J. Hatchwell ◽  
Philippa R. Gullett ◽  
Mark J. Adams

Inclusive fitness theory provides the conceptual framework for our current understanding of social evolution, and empirical studies suggest that kin selection is a critical process in the evolution of animal sociality. A key prediction of inclusive fitness theory is that altruistic behaviour evolves when the costs incurred by an altruist ( c ) are outweighed by the benefit to the recipient ( b ), weighted by the relatedness of altruist to recipient ( r ), i.e. Hamilton's rule rb > c . Despite its central importance in social evolution theory, there have been relatively few empirical tests of Hamilton's rule, and hardly any among cooperatively breeding vertebrates, leading some authors to question its utility. Here, we use data from a long-term study of cooperatively breeding long-tailed tits Aegithalos caudatus to examine whether helping behaviour satisfies Hamilton's condition for the evolution of altruism. We show that helpers are altruistic because they incur survival costs through the provision of alloparental care for offspring. However, they also accrue substantial benefits through increased survival of related breeders and offspring, and despite the low average relatedness of helpers to recipients, these benefits of helping outweigh the costs incurred. We conclude that Hamilton's rule for the evolution of altruistic helping behaviour is satisfied in this species.


2019 ◽  
Vol 374 (1769) ◽  
pp. 20180412 ◽  
Author(s):  
M. Polačik ◽  
M. Reichard ◽  
C. Smith ◽  
R. Blažek

Interspecific brood parasitism occurs in several independent lineages of birds and social insects, putatively evolving from intraspecific brood parasitism. The cuckoo catfish, Synodontis multipunctatus , the only known obligatory non-avian brood parasite, exploits mouthbrooding cichlid fishes in Lake Tanganyika, despite the absence of parental care in its evolutionary lineage (family Mochokidae). Cuckoo catfish participate in host spawning events, with their eggs subsequently collected and brooded by parental cichlids, though they can later be selectively rejected by the host. One scenario for the origin of brood parasitism in cuckoo catfish is through predation of cichlid eggs during spawning, eventually resulting in a spatial and temporal match in oviposition by host and parasite. Here we demonstrate experimentally that, uniquely among all known brood parasites, cuckoo catfish have the capacity to re-infect their hosts at a late developmental stage following egg rejection. We show that cuckoo catfish offspring can survive outside the host buccal cavity and re-infect parental hosts at a later incubation phase by exploiting the strong parental instinct of hosts to collect stray offspring. This finding implies an alternative evolutionary origin for cuckoo catfish brood parasitism, with the parental response of host cichlids facilitating its evolution. This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.


2021 ◽  
Author(s):  
Matthew H J Chaumont ◽  
Naomi E Langmore ◽  
Justin A Welbergen

Abstract Coevolutionary arms races between brood parasites and hosts provide tractable systems for understanding antagonistic coevolution in nature; however, little is known about the fate of frontline antiparasite defences when the host ‘wins’ the coevolutionary arms race. By recreating bygone species-interactions, using artificial parasitism experiments, lingering defensive behaviors that evolved in the context of parasitism can be understood and may even be used to identify the unknown agent of parasitism past. Here we present the first study of this type by evaluating lingering “frontline” nest defences that have evolved to prevent egg laying in a former brood parasite host. The Australian reed warbler Acrocephalus australis, is currently not parasitized but is known to exhibit fine-tuned egg discrimination—a defensive behavior indicative of a past brood parasite-host arms race and common in closely related parasitized species. Here, using 3 D-printed models of adult brood parasites, we examined whether the Australian reed warbler also exhibits frontline defences to adult brood parasites, and whether we could use these defences to identify the warbler’s “ghost of parasitism past”. Our findings provide evidence that the Australian reed warbler readily engages in frontline defences that are considered adaptive specifically in the context of brood parasitism. However, individuals were unable to discriminate between adults of different brood parasite species at their nest. Overall, our results demonstrate that despite a relaxation in selection, defences against brood parasitism can be maintained across multiple stages of the host’s nesting cycle, and further suggest that, in accordance with previous findings, that learning may be important for fine-tuning frontline defence.


2019 ◽  
Vol 374 (1769) ◽  
pp. 20180196 ◽  
Author(s):  
Jessica R. Litman

Brood parasitism is a specialized form of parasitism in which the offspring of a parasite develops on the food provisions gathered by a host species for its own young. Obligate brood parasitic lineages have lost the ability to acquire provisions for their young and thus rely entirely on the location of an appropriate host to serve as a food-provider. Solitary bees provide some of the most fascinating examples of brood parasitism in animals. Most solitary bees build and provision their own nests. Some, however, usurp the nests of other species of bees. These brood parasites, or ‘cuckoo’ bees, deposit their eggs on the pollen provisions collected by a host bee for her own offspring. The provisions stored by the host bee are not sufficient to sustain the development of both the host's larva and that of the brood parasite and the parasite must kill the offspring of its host in order to obtain enough nourishment to complete its development. As a consequence, there is fierce competition between the host bee seeking to protect her nest from attack and the brood parasite seeking to avoid detection by the host in order to successfully deposit her eggs in an appropriate nest. In this paper, I review the behaviours that allow brood parasitic bees to escape detection by their hosts. Identifying these behaviours, and placing them within the general context of strategies employed by brood parasitic bees to parasitize the nests of their hosts, is key to understanding how brood parasitic lineages may have evolved from nest-building ancestors, decrypting the selective pressures that drive evolutionary transitions from one strategy to another and, more broadly, revealing how similar selective pressures in widely divergent lineages of animals have given rise to remarkably convergent behaviours. This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.


2019 ◽  
Vol 374 (1769) ◽  
pp. 20180207 ◽  
Author(s):  
S. C. Cotter ◽  
D. Pincheira-Donoso ◽  
R. Thorogood

Parasitic interactions are so ubiquitous that all multicellular organisms have evolved a system of defences to reduce their costs, whether the parasites they encounter are the classic parasites which feed on the individual, or brood parasites which usurp parental care. Many parallels have been drawn between defences deployed against both types of parasite, but typically, while defences against classic parasites have been selected to protect survival, those against brood parasites have been selected to protect the parent's inclusive fitness, suggesting that the selection pressures they impose are fundamentally different. However, there is another class of defences against classic parasites that have specifically been selected to protect an individual's inclusive fitness, known as social immunity . Social immune responses include the anti-parasite defences typically provided for others in kin-structured groups, such as the antifungal secretions produced by termite workers to protect the brood. Defences against brood parasites, therefore, are more closely aligned with social immune responses. Much like social immunity, host defences against brood parasitism are employed by a donor (a parent) for the benefit of one or more recipients (typically kin), and as with social defences against classic parasites, defences have therefore evolved to protect the donor's inclusive fitness, not the survival or ultimately the fitness of individual recipients This can lead to severe conflicts between the different parties, whose interests are not always aligned. Here, we consider defences against brood parasitism in the light of social immunity, at different stages of parasite encounter, addressing where conflicts occur and how they might be resolved. We finish with considering how this approach could help us to address longstanding questions in our understanding of brood parasitism. This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.


Author(s):  
Kristen Noel ◽  
Rodger Titman ◽  
Shawn R. Craik

Conspecific brood parasitism (CBP) has been observed in approximately half of all species of waterfowl, a philopatric group in which breeding females are frequently locally related. It has been suggested that kin selection can facilitate the evolution of CBP in waterfowl via fitness benefits for the host and parasite. One model demonstrates that discrimination of related and unrelated parasites by the host must be sufficient for kinship to promote CBP, provided that costs of brood parasitism to host fitness are sufficiently low. We parameterized the model using demographic data and behavioural observations from a population of colonial Red-breasted Mergansers (Mergus serrator (Linnaeus, 1758)) in which 47% of nests were parasitized by conspecifics. The costs of 1-3 foreign eggs to host hatching success were generally small (decline of 1.8% per additional egg). Nevertheless, model outputs revealed that brood parasites maximize their inclusive fitness by avoiding nests of relatives, primarily because of constraints on a host’s ability to detect parasites at the nest. Indeed, hosts spent <8% of the diurnal period at the nest during egg laying, a period when parasite activity is greatest. It is thus highly unlikely that relatedness and kin selection promote brood parasitism in this population.


2006 ◽  
Vol 274 (1610) ◽  
pp. 713-719 ◽  
Author(s):  
Alan Grafen

A recent model shows that altruism can evolve with limited migration and variable group sizes, and the authors claim that kin selection cannot provide a sufficient explanation of their results. It is demonstrated, using a recent reformulation of Hamilton's original arguments, that the model falls squarely within the scope of inclusive fitness theory, which furthermore shows how to calculate inclusive fitness and the relevant relatedness. A distinction is drawn between inclusive fitness, which is a method of analysing social behaviour; and kin selection, a process that operates through genetic similarity brought about by common ancestry, but not by assortation by genotype or by direct assessment of genetic similarity. The recent model is analysed, and it turns out that kin selection provides a sufficient explanation to considerable quantitative accuracy, contrary to the authors' claims. A parallel analysis is possible and would be illuminating for all models of social behaviour in which individuals' effects on each other's offspring numbers combine additively.


Author(s):  
Václav Jelínek ◽  
Michal Šulc ◽  
Gabriela Štětková ◽  
Marcel Honza

ABSTRACTAvian brood parasites pose a serious threat for hosts, substantially reducing their fitness which selects for the evolution of host defences. A classic example of a host frontline defence is mobbing which frequently includes contact attacking of brood parasites. Here, we investigated how the nest defence of a very aggressive great reed warbler (Acrocephalus arundinaceus) host influences the speed of egg-laying and egg-removing behaviour of its brood parasite – the common cuckoo (Cuculus canorus). We video-recorded 168 brood parasitic events at 102 active host nests and found that cuckoos avoided host mobbing in only 62% of cases. If hosts spotted the cuckoo at their nests, they almost always attacked it (in 91 of 104 cases), however, such attacks only rarely and temporarily prevented cuckoos from parasitizing (11 additional cases). When attacked, cuckoos parasitized host nests significantly faster and left them immediately. However, when not attacked, cuckoos frequently stayed at or near the nest suggesting that host aggression, rather than the risk of being spotted, influences the speed of brood parasitism in this species. Further, we found that cuckoos performed egg-removing behaviour in all parasitic events without regard to host aggression. As a result, cuckoos removed at least one egg during all brood parasitism events except those when an egg slipped from their beaks and fell back into the nest (in 9 of 73 cases). This indicates that egg-removing behaviour is not costly for the common cuckoo and is an essential part of its parasitism strategy, widening understanding of this currently unexplained behaviour.


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