Click
here to close Hello! We notice that
you are using Internet Explorer, which is not supported by Echinobase
and may cause the site to display incorrectly. We suggest using a
current version of Chrome,
FireFox,
or Safari.
Philos Trans R Soc Lond B Biol Sci
2021 Nov 08;3761837:20200366. doi: 10.1098/rstb.2020.0366.
Show Gene links
Show Anatomy links
Phanerozoic parasitism and marine metazoan diversity: dilution versus amplification.
De Baets K
,
Huntley JW
,
Scarponi D
,
Klompmaker AA
,
Skawina A
.
???displayArticle.abstract???
Growing evidence suggests that biodiversity mediates parasite prevalence. We have compiled the first global database on occurrences and prevalence of marine parasitism throughout the Phanerozoic and assess the relationship with biodiversity to test if there is support for amplification or dilution of parasitism at the macroevolutionary scale. Median prevalence values by era are 5% for the Paleozoic, 4% for the Mesozoic, and a significant increase to 10% for the Cenozoic. We calculated period-level shareholder quorum sub-sampled (SQS) estimates of mean sampled diversity, three-timer (3T) origination rates, and 3T extinction rates for the most abundant host clades in the Paleobiology Database to compare to both occurrences of parasitism and the more informative parasite prevalence values. Generalized linear models (GLMs) of parasite occurrences and SQS diversity measures support both the amplification (all taxa pooled, crinoids and blastoids, and molluscs) and dilution hypotheses (arthropods, cnidarians, and bivalves). GLMs of prevalence and SQS diversity measures support the amplification hypothesis (all taxa pooled and molluscs). Though likely scale-dependent, parasitism has increased through the Phanerozoic and clear patterns primarily support the amplification of parasitism with biodiversity in the history of life. This article is part of the theme issue 'Infectious disease macroecology: parasite diversity and dynamics across the globe'.
Figure 1. . Examples of parasite–host interactions preserved on marine animal host skeletons. (a) Modern isopod-infested decapod (as indicated by swelling on right side), Galathea sp. Camiguin, Philippines (Klompmaker et al. [77]; Creative Commons Attribution License). (b) Middle Devonian crinoid, Arthroacantha carpenteri, infested by platyceratid gastropod (placed on the topmost side of the picture), Silica Shale, Sylvania, Ohio, US (Baumiller & Gahn [32]; reproduced with permission). (c) Holocene trematode-induced circular pits on interior of bivalve Chamelea gallina, specimen 129 from 13.10 m depth sample of core 240S8, Po River plain, Italy (photomicrograph by JWH). (d) Modern death assemblage spionid polychaete-induced mudblister (right side) on bivalve Clinocardium nuttalli, Monroe Landing, Whidbey Island, Washington, USA (transmitted and reflected light photomicrograph; JWH collections: photomicrograph by Gabriel S Jacobs). (e) Early Cambrian encrusting tubes of unknown kleptoparasite on the brachiopod Neobolus wulongqingensis, Guanshan Konservat-Lagerstatte, Wulongqing Formation, eastern Yunnan, China (Zhang et al. [41]; Creative Commons Attribution 4.0 International License).
Figure 2. . Phanerozoic history of parasitism occurrence and prevalence among marine animals. (a) Rug plot (along x-axis) and density plot of the temporal distribution of single host taxon occurrences through geologic time. (b) Prevalence values of occurrences with at least 10 specimens through geologic time colour-coded by host phylum. Inset plot, median prevalence values by era.
Figure 3. . Graphical depiction of GLM of occurrences (y-axes) versus SQS mean standing diversity, SQS 3T origination rates, 3T extinction rates, and midpoint age of geologic time period (as reported in table 1). The solid line depicts the resulting generalized linear model and the grey field represents its 95% confidence interval. (Online version in colour.)
Figure 4. . Graphical depiction of GLM of prevalence values (y-axes) versus SQS mean standing diversity, SQS 3T origination rates, SQS 3T extinction rates and best estimate age of sample (as reported in table 3). The solid line depicts the resulting generalized linear model and the grey field represents its 95% confidence interval. (Online version in colour.)
Alroy,
The shifting balance of diversity among major marine animal groups.
2010, Pubmed
Alroy,
The shifting balance of diversity among major marine animal groups.
2010,
Pubmed
Alroy,
Effects of sampling standardization on estimates of Phanerozoic marine diversification.
2001,
Pubmed
Alroy,
Phanerozoic trends in the global diversity of marine invertebrates.
2008,
Pubmed
Auld,
The evolutionary ecology of complex lifecycle parasites: linking phenomena with mechanisms.
2015,
Pubmed
Barnes,
Global patterns in predator-prey size relationships reveal size dependency of trophic transfer efficiency.
2010,
Pubmed
Benesh,
The trophic vacuum and the evolution of complex life cycles in trophically transmitted helminths.
2014,
Pubmed
Bengtson,
Predatorial borings in late precambrian mineralized exoskeletons.
1992,
Pubmed
Boast,
Coprolites reveal ecological interactions lost with the extinction of New Zealand birds.
2018,
Pubmed
Carlson,
Parasite biodiversity faces extinction and redistribution in a changing climate.
2017,
Pubmed
Civitello,
Biodiversity inhibits parasites: Broad evidence for the dilution effect.
2015,
Pubmed
Cressey,
Fossil parasitic copepods from a lower cretaceous fish.
1973,
Pubmed
Dallas,
Spatial variation in species' roles in host-helminth networks.
2021,
Pubmed
De Baets,
The Importance of Fossils in Understanding the Evolution of Parasites and Their Vectors.
2015,
Pubmed
De Baets,
Phanerozoic parasitism and marine metazoan diversity: dilution versus amplification.
2021,
Pubmed
,
Echinobase
Dobson,
Colloquium paper: homage to Linnaeus: how many parasites? How many hosts?
2008,
Pubmed
Dunn,
The sixth mass coextinction: are most endangered species parasites and mutualists?
2009,
Pubmed
Farrell,
The ghost of hosts past: impacts of host extinction on parasite specificity.
2021,
Pubmed
Faust,
Null expectations for disease dynamics in shrinking habitat: dilution or amplification?
2017,
Pubmed
Fraser,
Investigating Biotic Interactions in Deep Time.
2021,
Pubmed
Halliday,
Measuring the shape of the biodiversity-disease relationship across systems reveals new findings and key gaps.
2019,
Pubmed
Halliday,
Biodiversity loss underlies the dilution effect of biodiversity.
2020,
Pubmed
Harley,
Climate change, keystone predation, and biodiversity loss.
2011,
Pubmed
,
Echinobase
Herrera,
Predictions of primate-parasite coextinction.
2021,
Pubmed
Huang,
The diversity-disease relationship: evidence for and criticisms of the dilution effect.
2016,
Pubmed
Huntley,
Strong coupling of predation intensity and diversity in the Phanerozoic fossil record.
2007,
Pubmed
Huntley,
Trace Fossil Evidence of Trematode-Bivalve Parasite-Host Interactions in Deep Time.
2015,
Pubmed
Jablonski,
Biotic interactions and macroevolution: extensions and mismatches across scales and levels.
2008,
Pubmed
Johnson,
Diversity, decoys and the dilution effect: how ecological communities affect disease risk.
2010,
Pubmed
Klompmaker,
Increase in predator-prey size ratios throughout the Phanerozoic history of marine ecosystems.
2017,
Pubmed
Klompmaker,
Parasites in the fossil record: a Cretaceous fauna with isopod-infested decapod crustaceans, infestation patterns through time, and a new ichnotaxon.
2014,
Pubmed
Leung,
Fossils of parasites: what can the fossil record tell us about the evolution of parasitism?
2017,
Pubmed
Madin,
Statistical independence of escalatory ecological trends in Phanerozoic marine invertebrates.
2006,
Pubmed
Magnusson,
Effect of spatial scale and latitude on diversity-disease relationships.
2020,
Pubmed
Martins,
Drivers of parasite β-diversity among anuran hosts depend on scale, realm and parasite group.
2021,
Pubmed
Monk,
Ecological constraints on the origin of neurones.
2015,
Pubmed
Poulin,
Functional biogeography of parasite traits: hypotheses and evidence.
2021,
Pubmed
Randle,
Bite marks and predation of fossil jawless fish during the rise of jawed vertebrates.
2019,
Pubmed
Randolph,
Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm.
2012,
Pubmed
Riascos,
Long-term parasitic association between the boring polychaete Polydora bioccipitalis and Mesodesma donacium.
2009,
Pubmed
Rohr,
Predator diversity, intraguild predation, and indirect effects drive parasite transmission.
2015,
Pubmed
Salkeld,
A meta-analysis suggesting that the relationship between biodiversity and risk of zoonotic pathogen transmission is idiosyncratic.
2013,
Pubmed
Sallan,
Persistent predator-prey dynamics revealed by mass extinction.
2011,
Pubmed
,
Echinobase
Seilacher,
The parasite connection in ecosystems and macroevolution.
2007,
Pubmed
Sepkoski,
Biodiversity: past, present, and future.
1997,
Pubmed
Shields,
The impact of pathogens on exploited populations of decapod crustaceans.
2012,
Pubmed
Smith,
Large-scale heterogeneity of the fossil record: implications for Phanerozoic biodiversity studies.
2001,
Pubmed
Sonnenholzner,
Food webs and fishing affect parasitism of the sea urchin Eucidaris galapagensis in the Galápagos.
2011,
Pubmed
,
Echinobase
Sperling,
Oxygen, ecology, and the Cambrian radiation of animals.
2013,
Pubmed
Strona,
Past, present and future of host-parasite co-extinctions.
2015,
Pubmed
Strydom,
A roadmap towards predicting species interaction networks (across space and time).
2021,
Pubmed
Su,
How intraguild predation affects the host diversity-disease relationship in a multihost community.
2020,
Pubmed
Voje,
The role of biotic forces in driving macroevolution: beyond the Red Queen.
2015,
Pubmed
Wang,
Intraguild predation enhances biodiversity and functioning in complex food webs.
2019,
Pubmed
Weinstein,
Independent origins of parasitism in Animalia.
2016,
Pubmed
Wood,
Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission.
2013,
Pubmed
Zapalski,
First fossil record of parasitism in Devonian calcareous sponges (stromatoporoids).
2011,
Pubmed
Zhang,
An encrusting kleptoparasite-host interaction from the early Cambrian.
2020,
Pubmed