Evolution of the Gene Network Underlying Wing Polyphenism in Ants

Abouheif, Ehab; Wray, Gregory A.

doi:10.1126/science.1071468

Cited by 369 publications

(393 citation statements)

References 14 publications

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“…Third, the transition to obligate eusociality requires further evolution or elaboration of caste-specific gene expression, for example through gene duplications, to reduce the relative significance of the original pleiotropic genes that affect both helper and breeder performance. Whereas it is easy to see how the first two steps apply to cooperative breeders such as Polistes wasps, step 3 requires a long process of directional selection for decoupling the expression of genes coding for maternal and sibling care and for these alternative phenotypes to become associated with an early developmental bifurcation and correlated with the expression of novel mutations at other loci so that permanent morphological castes emerge (Hunt 1994;West Eberhard 1996;Abouheif & Wray 2002;Linksvayer & Wade 2005;Wilson 2008). Recent evidence has demonstrated the key significance of nutrition for caste determination (Hunt 2007), providing direct insights into the proximate factors that characterize transitions to obligate eusociality.…”

Section: Discussionmentioning

confidence: 99%

Lifetime monogamy and the evolution of eusociality

Boomsma

2009

Phil. Trans. R. Soc. B

324

378

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All evidence currently available indicates that obligatory sterile eusocial castes only arose via the association of lifetime monogamous parents and offspring. This is consistent with Hamilton's rule (br s . r o c), but implies that relatedness cancels out of the equation because average relatedness to siblings (r s ) and offspring (r o ) are both predictably 0.5. This equality implies that any infinitesimally small benefit of helping at the maternal nest (b), relative to the cost in personal reproduction (c) that persists throughout the lifespan of entire cohorts of helpers suffices to establish permanent eusociality, so that group benefits can increase gradually during, but mostly after the transition. The monogamy window can be conceptualized as a singularity comparable with the single zygote commitment of gametes in eukaryotes. The increase of colony size in ants, bees, wasps and termites is thus analogous to the evolution of multicellularity. Focusing on lifetime monogamy as a universal precondition for the evolution of obligate eusociality simplifies the theory and may help to resolve controversies about levels of selection and targets of adaptation. The monogamy window underlines that cooperative breeding and eusociality are different domains of social evolution, characterized by different sectors of parameter space for Hamilton's rule.

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Section: Discussionmentioning

confidence: 99%

Lifetime monogamy and the evolution of eusociality

Boomsma

2009

Phil. Trans. R. Soc. B

324

378

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“…One form of flexibility is phenotypic plasticity in which a phenotype changes when the environment changes. The norm of reaction, which is a systematic change in phenotype along an environmental gradient (Schlichting and Pigliucci 1998), is an example of phenotypic plasticity, as is polyphenism, the development of alternative phenotypes in response to environmental signals (Pfennig 1992;Nijhout 1999Nijhout , 2003Abouheif and Wray 2002;Moczek and Nijhout 2003;Simpson and Sword 2009).…”

Section: Mechanisms Of Robustnessmentioning

confidence: 99%

Systems Biology of Phenotypic Robustness and Plasticity

Nijhout

Sadre-Marandi

Best

et al. 2017

Integrative and Comparative Biology

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Synopsis Gene regulatory networks, cellular biochemistry, tissue function, and whole body physiology are imbued with myriad overlapping and interacting homeostatic mechanisms that ensure that many phenotypes are robust to genetic and environmental variation. Animals also often have plastic responses to environmental variables, which means that many different phenotypes can correspond to a single genotype. Since natural selection acts on phenotypes, this raises the question of how selection can act on the genome if genotypes are decoupled from phenotypes by robustness and plasticity mechanisms. The answer can be found in the systems biology of the homeostatic mechanisms themselves. First, all such mechanisms operate over a limited range and outside that range the controlled variable changes rapidly allowing natural selection to act. Second, mutations and environmental stressors can disrupt homeostatic mechanisms, exposing cryptic genetic variation and allowing natural selection to act. We illustrate these ideas by examining the systems biology of four specific examples. We show how it is possible to analyze and visualize the roles of specific genes and specific polymorphisms in robustness in the context of large and realistic nonlinear systems. We also describe a new method, system population models, that allows one to connect causal dynamics to the variable outcomes that one sees in biological populations with large variation.

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“…Often, however, new bodyplans also emerge by the loss of features and organs. Examples of this so-called regressive evolution include eye loss in cavefish [1], wing loss in ants [2] or the loss of limbs in the snake bodyplan [3]. Another textbook example for regressive evolution is limb loss on the intercalary segment in insects [4].…”

Section: Introductionmentioning

confidence: 99%

Regressive evolution of the arthropod tritocerebral segment linked to functional divergence of the Hox genelabial

et al. 2015

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The intercalary segment is a limbless version of the tritocerebral segment and is present in the head of all insects, whereas other extant arthropods have retained limbs on their tritocerebral segment (e.g. the pedipalp limbs in spiders). The evolutionary origin of limb loss on the intercalary segment has puzzled zoologists for over a century. Here we show that an intercalary segment-like phenotype can be created in spiders by interfering with the function of the Hox gene labial. This links the origin of the intercalary segment to a functional change in labial. We show that in the spider Parasteatoda tepidariorum the labial gene has two functions: one function in head tissue maintenance that is conserved between spiders and insects, and a second function in pedipalp limb promotion and specification, which is only present in spiders. These results imply that labial was originally crucial for limb formation on the tritocerebral segment, but that it has lost this particular subfunction in the insect ancestor, resulting in limb loss on the intercalary segment. Such loss of a subfunction is a way to avoid adverse pleiotropic effects normally associated with mutations in developmental genes, and may thus be a common mechanism to accelerate regressive evolution.

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Evolution of the Gene Network Underlying Wing Polyphenism in Ants

Cited by 369 publications

References 14 publications

Lifetime monogamy and the evolution of eusociality

Lifetime monogamy and the evolution of eusociality

Systems Biology of Phenotypic Robustness and Plasticity

Regressive evolution of the arthropod tritocerebral segment linked to functional divergence of the Hox genelabial

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