Defensive traits exhibit an evolutionary trade-off and drive diversification in ants

Blanchard, Benjamin D.

doi:10.1603/ice.2016.111679

Cited by 17 publications

(23 citation statements)

References 85 publications

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“…These predictions set a course for the integrated understanding of colony function as arising from nestmate specialization and decentralized physiological processes that have been shaped by millions of years of colony-level selection. All predictions and hypotheses should be carried out within a phylogenetic comparative framework to disentangle the relative importance of genomic, ecological, and behavioral constraints over evolutionary time 1,30,141,142 . Table 1 .…”

Section: Predictions For Eusocial Colony Physiologymentioning

confidence: 99%

Distributed physiology and the molecular basis of social life in eusocial insects

Friedman

Johnson

Linksvayer

2020

Hormones and Behavior

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The traditional focus of physiological and functional genomic research is on molecular processes that play out within a single body. In contrast, when social interactions occur, molecular and behavioral responses in interacting individuals can lead to physiological processes that are distributed across multiple individuals. In eusocial insect colonies, such multi-body processes are tightly integrated, involving social communication mechanisms that regulate the physiology of colony members. As a result, conserved physiological mechanisms, for example related to pheromone detection and neural signaling pathways, are deployed in novel contexts and regulate emergent colony traits during the evolutionary origin and elaboration of social complexity. Here we review conceptual frameworks for organismal and colony physiology, and highlight functional genomic, physiological, and behavioral research exploring how colony-level traits arise from physical and chemical interactions among nestmates. We highlight mechanistic work exploring how colony traits arise from physical and chemical interactions among physiologically-specialized nestmates of 1 various developmental stages. We consider similarities and differences between organismal and colony physiology, and make specific predictions based on a decentralized perspective on the function and evolution of colony traits. Integrated models of colony physiological function will be useful to address fundamental questions related to the evolution and ecology of collective behavior in natural systems. Colony Organization = Social Anatomy + Social PhysiologyEusocial colonial insects, such as ants, termites, and honey bees, thrive across almost all terrestrial ecosystems 1,2 . The ecological success of these species rests in their use of colony traits, such as nest architecture 3,4 and collective foraging behavior 5-7 , which are functionally absent in solitary insects yet keenly developed in eusocial taxa. In the eusocial insects, division of labor (DOL) describes how nestmates vary in their form and function. DOL formalizes the extent of specialization among nestmates in the performance of tasks, usually with a physiological or morphological basis or arising from nestmate age (temporal polyethism) and experience [8][9][10][11] . We build off of the conceptual framework of Johnson & Linksvayer 12 that considers eusocial colony organization from the perspective of social anatomy & social physiology : Social anatomy is the notion that colonies are composed of specialized parts with limited roles, like the organs of an individual animal. Specialized colony anatomy allows for greater productivity and efficiency for the completion of many tasks.Physiological specialization exists at multiple levels within the colony. Queen-worker specialization allows for an increased reproductive output of queens alongside increased work output from workers, from the same diploid female genome 13 .Subspecialization among workers can manifest as permanent variation in body morphology 14 , temporal polyet...

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Section: Predictions For Eusocial Colony Physiologymentioning

confidence: 99%

Distributed physiology and the molecular basis of social life in eusocial insects

Friedman

Johnson

Linksvayer

2020

Hormones and Behavior

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“…Although state-dependent diversification and unequal transition rates between states have frequently been documented (e.g., Tripp and Manos 2008;Goldberg et al 2010;Beaulieu and Donoghue 2013;Weber and Agrawal 2014;Blanchard and Moreau 2017;Nakov et al 2017), we are just beginning to understand how these processes combine to explain extant patterns of diversity . One current limitation in distinguishing equilibrium and nonequilibrium explanations for trait rarity is a lack of appropriate tools.…”

Section: Impact Summarymentioning

confidence: 99%

Adaptation to hummingbird pollination is associated with reduced diversification inPenstemon

2019

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A striking characteristic of the Western North American flora is the repeated evolution of hummingbird pollination from insect‐pollinated ancestors. This pattern has received extensive attention as an opportunity to study repeated trait evolution as well as potential constraints on evolutionary reversibility, with little attention focused on the impact of these transitions on species diversification rates. Yet traits conferring adaptation to divergent pollinators potentially impact speciation and extinction rates, because pollinators facilitate plant reproduction and specify mating patterns between flowering plants. Here, we examine macroevolutionary processes affecting floral pollination syndrome diversity in the largest North American genus of flowering plants, Penstemon. Within Penstemon, transitions from ancestral bee‐adapted flowers to hummingbird‐adapted flowers have frequently occurred, although hummingbird‐adapted species are rare overall within the genus. We inferred macroevolutionary transition and state‐dependent diversification rates and found that transitions from ancestral bee‐adapted flowers to hummingbird‐adapted flowers are associated with reduced net diversification rate, a finding based on an estimated 17 origins of hummingbird pollination in our sample. Although this finding is congruent with hypotheses that hummingbird adaptation in North American Flora is associated with reduced species diversification rates, it contrasts with studies of neotropical plant families where hummingbird pollination has been associated with increased species diversification. We further used the estimated macroevolutionary rates to predict the expected pattern of floral diversity within Penstemon over time, assuming stable diversification and transition rates. Under these assumptions, we find that hummingbird‐adapted species are expected to remain rare due to their reduced diversification rates. In fact, current floral diversity in the sampled Penstemon lineage, where less than one‐fifth of species are hummingbird adapted, is consistent with predicted levels of diversity under stable macroevolutionary rates.

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“…The evolution of either antipredator defences or predator avoidance mechanisms should reduce the selective pressures on the other, or the probability of evolution of the other. Evolutionary trade-offs in antipredator adaptations have been reported in other organismal groups (Losos et al 2002;Blanchard & Moreau 2017). Among fishes, such tradeoffs have been proposed (McLean & Godin 1989;Brainerd & Patek 1998) and supported by evidence at the population-level for a select number of fish species (Andraso & Barron 1995;Bergstrom 2002;Leinonen et al 2011).…”

Section: Solitary Facultative Grazermentioning

confidence: 78%

“…A number of studies have examined the microevolutionary effects of predation risk on adaptive trait changes in behaviour (reviewed in Lima 1998;Bednekoff 2007) and morphology (Br€ onmark & Miner 1992;Andersson et al 2006;Langerhans 2009;Frommen et al 2011). Few studies have examined the effects of predation risk on a macroevolutionary scale and considered the complexity of integrating gross morphological antipredator adaptations with behavioural decision-making (but see Blanchard & Moreau 2017).…”

Section: Introductionmentioning

confidence: 99%

Ecology shapes the evolutionary trade‐off between predator avoidance and defence in coral reef butterflyfishes

et al. 2018

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Antipredator defensive traits are thought to trade-off evolutionarily with traits that facilitate predator avoidance. However, complexity and scale have precluded tests of this prediction in many groups, including fishes. Using a macroevolutionary approach, we test this prediction in butterflyfishes, an iconic group of coral reef inhabitants with diverse social behaviours, foraging strategies and antipredator adaptations. We find that several antipredator traits have evolved adaptively, dependent primarily on foraging strategy. We identify a previously unrecognised axis of diversity in butterflyfishes where species with robust morphological defences have riskier foraging strategies and lack sociality, while species with reduced morphological defences feed in familiar territories, have adaptations for quick escapes and benefit from the vigilance provided by sociality. Furthermore, we find evidence for the constrained evolution of fin spines among species that graze solely on corals, highlighting the importance of corals, as both prey and structural refuge, in shaping fish morphology.

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Defensive traits exhibit an evolutionary trade-off and drive diversification in ants

Cited by 17 publications

References 85 publications

Distributed physiology and the molecular basis of social life in eusocial insects

Distributed physiology and the molecular basis of social life in eusocial insects

Adaptation to hummingbird pollination is associated with reduced diversification inPenstemon

Ecology shapes the evolutionary trade‐off between predator avoidance and defence in coral reef butterflyfishes

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