Evolutionary Ecology of Organs: A Missing Link in Cancer Development?

Thomas, Frédéric; Nesse, Randolph M.; Gatenby, Robert A.; Gidoin, Cindy; Renaud, François; Roche, Benjamín; Újvári, Beáta

doi:10.1016/j.trecan.2016.06.009

Cited by 36 publications

(35 citation statements)

References 39 publications

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“…Moreover, compelling evidence that phenotypic traits age differently might provide new insights on the complex relationships linking age-related diseases and aging trajectories. We can expect a selection for mechanisms that preferentially protect structures, functions, or organs that are the most important to maximize Darwinian fitness, as recently suggested in the context of cancer development (Thomas et al 2016).…”

Section: Prediction 5 "Senescence Should Always Be a Generalized Detmentioning

confidence: 87%

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The Williams' legacy: A critical reappraisal of his nine predictions about the evolution of senescence

2017

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Williams' evolutionary theory of senescence based on antagonistic pleiotropy has become a landmark in evolutionary biology, and more recently in biogerontology and evolutionary medicine. In his original article, Williams launched a set of nine "testable deductions" from his theory. Although some of these predictions have been repeatedly discussed, most have been overlooked and no systematic evaluation of the whole set of Williams' original predictions has been performed. For the sixtieth anniversary of the publication of the Williams' article, we provide an updated evaluation of all these predictions. We present the pros and cons of each prediction based on recent accumulation of both theoretical and empirical studies performed in the laboratory and in the wild. From our viewpoint, six predictions are mostly supported by our current knowledge at least under some conditions (although Williams' theory cannot thoroughly explain why for some of them). Three predictions, all involving the timing of senescence, are not supported. Our critical review of Williams' predictions highlights the importance of William's contribution and clearly demonstrates that, 60 years after its publication, his article does not show any sign of senescence.

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Section: Prediction 5 "Senescence Should Always Be a Generalized Detmentioning

confidence: 87%

“…We can expect a selection for mechanisms that preferentially protect structures, functions, or organs that are the most important to maximize Darwinian fitness, as recently suggested in the context of cancer development (Thomas et al. ).…”

Section: A Critical Appraisal Of Each Of the Nine Predictions Formulamentioning

confidence: 90%

The Williams' legacy: A critical reappraisal of his nine predictions about the evolution of senescence

2017

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“…It is also unclear how senescence in wild populations affects the overall odds of reproductive success, which is the key regulator of the age-dependent strength of germline selection. Recent evidence also indicates that different tissues in the body have different rates of aging [50], which might potentially be a contributor to the differential tissue-specific cancer risk. Finally, while still speculative, understanding cancer as being determined by evolved life history may help explain the earlier incidence of a number of cancers, such as brain, bowel, chronic myeloid leukemia, chronic lymphocytic leukemia and acute myeloid leukemia, in males relative to females (cancers which are neither sex-specific or substantially due to smoking were queried; Cancer Research UK; http://www.cancerresearchuk.org).…”

Section: The Evolution Of Lifespan As Key To Understanding Aging-relamentioning

confidence: 99%

The Evolution of Lifespan and Age-Dependent Cancer Risk

Rozhok

DeGregori

2016

Trends in Cancer

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The Armitage-Doll multi-stage model of carcinogenesis tremendously refocused cancer science by postulating that carcinogenesis is driven by a sequence of genetic changes in cells. Age-dependent cancer incidence thus has been explained in terms of the time necessary for oncogenic mutations to occur. While the multi-step nature of cancer evolution is well-supported by evidence, the mutation-centric theory is unable to explain a number of phenomena, such as the disproportion between cancer frequency and animal body size or the scaling of cancer incidence to animal lifespan. In this paper, we present a theoretical review of the current paradigm and discuss some fundamental evolutionary theory postulates that explain why cancer incidence is a function of lifespan and physiological, not chronological, aging.

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“…The first mechanism implies that the network structure has changed through time, because of carcinogenesis and cancer cell migration from novel primary sites, and/or metastasis to novel acceptor sites. Changes in tissue-level cancer risk may have an evolutionary basis ( 32, 48, 49) and/or be associated with novel environmental conditions (50) . The second mechanism is associated with preferential attachment, which in this context implies that a new primary tumor will likely metastasize in an acceptor organ with a high degree, and that a new metastasis is more likely to arise in a primary tumor that already metastasize to many different organs.…”

Section: Explaining the Observed Patternsmentioning

confidence: 99%

The network structure of cancer ecosystems

Castillo

Rebolledo

Arim

et al. 2017

Preprint

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Ever since Paget’s seed-and-soil and Ewing’s connectivity hypotheses to explain tumor metastasis (1,2), it has become clear that cancer progression can be envisaged as an ecological phenomenon. This connection has flourished during the past two decades (3–7), giving rise to important insights into the ecology and evolution of cancer progression, with therapeutic implications (8–10). Here, we take a metapopulation view of metastasis (i.e. the migration to and colonization of, habitat patches) and represent it as a bipartite network, distinguishing source patches, or organs that host a primary tumor, and acceptor patches, or organs colonized ultimately from the source through metastasis. Using 20,326, biomedical records obtained from literature, we show that: (i) the network structure of cancer ecosystems is non-random, exhibiting a nested subset pattern as has been found both in the distribution of species across islands and island-like habitats (11–13), and in the distribution of among species interactions across different ecological networks (14–16); (ii) similar to ecological networks, there is a heterogeneous distribution of degree (i.e., number of connections associated with a source or acceptor organ); (iii) there is a significant correlation between metastatic incidence (or the frequency with which tumor cells from a source organ colonize an acceptor one) and arterial blood supply, suggesting that more irrigated organs have a higher probability of developing metastasis or being invaded; (iv) there is a positive correlation between metastatic incidence and acceptor organ degree (or number of different tumor-bearing source organs that generate metastasis in a given acceptor organ), and a negative one between acceptor organ degree and number of stem cell divisions, implying that there are preferred sink organs for metastasis and that this could be related to average acceptor organ cell longevity; (v) there is a negative association between organ cell turnover and source organ degree, implying that organs with rapid cell turnovers tend to generate more metastasis, a process akin to the phenomenon of propagule pressure in ecology (17); and (vi) the cancer ecosystem network exhibits a modular structure in both source and acceptor patches, suggesting that some of them share more connections among themselves than with the rest of the network. We show that both niche-related processes occurring at the organ level as well as spatial connectivity and propagule pressure contribute to metastaticspread and result in a non-random cancer network, which exhibits a truncated power law degree distribution, clustering and a nested subset structure. The similarity between the cancer network and ecological networks highlights the importance of ecological approaches in increasing our understanding of patterns in cancer incidence and dynamics, which may lead to new strategies to control tumor spread within the human ecosystem.

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Evolutionary Ecology of Organs: A Missing Link in Cancer Development?

Cited by 36 publications

References 39 publications

The Williams' legacy: A critical reappraisal of his nine predictions about the evolution of senescence

The Williams' legacy: A critical reappraisal of his nine predictions about the evolution of senescence

The Evolution of Lifespan and Age-Dependent Cancer Risk

The network structure of cancer ecosystems

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