Title: Comparative demography elucidates the longevity of parasitic and symbiotic relationships

Journal Article · · Proceedings of the Royal Society B: Biological Sciences
 [1]; ORCiD logo [1];  [2]
  1. Oak Ridge Inst. for Science and Education (ORISE), Oak Ridge, TN (United States); U.S. Dept. of Agriculture, Beltsville, MD (United States)
  2. U.S. Dept. of Agriculture, Beltsville, MD (United States)

Parasitic and symbiotic relationships govern vast nutrient and energy flows, yet controversy surrounds their longevity. Enduring relationships may engender parallel phylogenies among hosts and parasites, but so may ephemeral relationships when parasites colonize related hosts. An understanding of whether symbiont and host populations have grown and contracted in concert would be useful when considering the temporal durability of these relationships. Here, we devised methods to compare demographic histories derived from genomic data. We compared the historical growth of the agent of severe human malaria, Plasmodium falciparum, and its mosquito vector, Anopheles gambiae, to human and primate histories, thereby discerning long-term parallels and anthropogenic population explosions. The growth history of Trichinella spiralis, a zoonotic parasite disseminated by swine, proved regionally specific, paralleling distinctive growth histories for wild boar in Asia and Europe. Parallel histories were inferred for an anemone and its algal symbiont (Exaiptasia pallida and Symbiodinium minutum). Concerted growth in potatoes and the agent of potato blight (Solanum tuberosum and Phytophthora infestans) did not commence until the age of potato domestication. Through these examples, we illustrate the utility of comparative historical demography as a new exploratory tool by which to interrogate the origins and durability of myriad ecological relationships. To facilitate future use of this approach, we introduce a tool called C-PSMC to align and evaluate the similarity of demographic history curves.

Research Organization:
Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE
Grant/Contract Number:
SC0014664
OSTI ID:
1580730
Journal Information:
Proceedings of the Royal Society B: Biological Sciences, Journal Name: Proceedings of the Royal Society B: Biological Sciences Journal Issue: 1888 Vol. 285; ISSN 0962-8452
Publisher:
The Royal Society PublishingCopyright Statement
Country of Publication:
United States
Language:
English

References (78)

Draft Assembly of the Symbiodinium minutum Nuclear Genome Reveals Dinoflagellate Gene Structure journal August 2013
Human dispersal of Trichinella spiralis in domesticated pigs journal December 2008
Coalescent genealogy samplers: windows into population history journal February 2009
Trees within trees: phylogeny and historical associations journal September 1998
Phylogenetic trees support the coevolution of parasites and their hosts journal March 1988
On the importance of being structured: instantaneous coalescence rates and human evolution—lessons for ancestral population size inference? journal December 2015
Genome sequence and analysis of the tuber crop potato journal January 2011
Inference of human population history from individual whole-genome sequences journal July 2011
Great ape genetic diversity and population history journal July 2013
African origin of the malaria parasite Plasmodium vivax journal February 2014
Whole-genome sequencing of the snub-nosed monkey provides insights into folivory and evolutionary history journal November 2014
Robust and scalable inference of population history from hundreds of unphased whole genomes journal December 2016
Genealogical trees, coalescent theory and the analysis of genetic polymorphisms journal May 2002
Examination of species boundaries in the Acropora cervicornis group (Scleractinia, Cnidaria) using nuclear DNA sequence analyses journal September 2000
Post-Miocene expansion, colonization, and host switching drove speciation among extant nematodes of the archaic genus Trichinella journal May 2006
The genome of Aiptasia , a sea anemone model for coral symbiosis journal August 2015
Evolution in Mendelian Populations journal March 1931
The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change journal June 2006
Investigating the causes and consequences of symbiont shuffling in a multi-partner reef coral symbiosis under environmental change journal June 2015
Approximating the coalescent with recombination journal July 2005
A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host-parasite systems journal September 2008
The Genome Sequence of the Malaria Mosquito Anopheles gambiae journal October 2002
Early Origin and Recent Expansion of Plasmodium falciparum journal April 2003
A Common Scaling Rule for Abundance, Energetics, and Production of Parasitic and Free-Living Species journal July 2011
Genomic signatures of population decline in the malaria mosquito Anopheles gambiae journal March 2016
Potential Costs of Acclimatization to a Warmer Climate: Growth of a Reef Coral with Heat Tolerant vs. Sensitive Symbiont Types journal May 2010
Trees within trees: phylogeny and historical associations journal September 1998
Draft Assembly of the Symbiodinium minutum Nuclear Genome Reveals Dinoflagellate Gene Structure journal August 2013
A combined mitochondrial and nuclear multilocus phylogeny of the genus Phytophthora journal May 2014
Human dispersal of Trichinella spiralis in domesticated pigs journal December 2008
Coalescent genealogy samplers: windows into population history journal February 2009
Glacial conditions in the Red Sea journal October 1994
Phylogenetic trees support the coevolution of parasites and their hosts journal March 1988
On the importance of being structured: instantaneous coalescence rates and human evolution—lessons for ancestral population size inference? journal December 2015
The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla journal August 2007
Ecosystem energetic implications of parasite and free-living biomass in three estuaries journal July 2008
Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans journal September 2009
Origin of the human malaria parasite Plasmodium falciparum in gorillas journal September 2010
Genome sequence and analysis of the tuber crop potato journal January 2011
Inference of human population history from individual whole-genome sequences journal July 2011
Analyses of pig genomes provide insight into porcine demography and evolution journal November 2012
Great ape genetic diversity and population history journal July 2013
Whole-genome sequencing of the snub-nosed monkey provides insights into folivory and evolutionary history journal November 2014
Robust and scalable inference of population history from hundreds of unphased whole genomes journal December 2016
The draft genome of the parasitic nematode Trichinella spiralis journal February 2011
Genealogical trees, coalescent theory and the analysis of genetic polymorphisms journal May 2002
Romanian wild boars and Mangalitza pigs have a European ancestry and harbour genetic signatures compatible with past population bottlenecks journal July 2016
Examination of species boundaries in the Acropora cervicornis group (Scleractinia, Cnidaria) using nuclear DNA sequence analyses journal September 2000
Post-Miocene expansion, colonization, and host switching drove speciation among extant nematodes of the archaic genus Trichinella journal May 2006
The origin of malignant malaria journal August 2009
The genome of Aiptasia , a sea anemone model for coral symbiosis journal August 2015
Phylogeny of the malarial genus Plasmodium, derived from rRNA gene sequences. journal November 1994
Malaria's Eve: Evidence of a recent population bottleneck throughout the world populations of Plasmodium falciparum journal April 1998
The Population Structure of Antibiotic-Producing Bacterial Symbionts of Apterostigma dentigerum Ants: Impacts of Coevolution and Multipartite Symbiosis journal November 2012
Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data journal April 2012
Evolution in Mendelian Populations journal March 1931
Spontaneous Mutation Rate in the Smallest Photosynthetic Eukaryotes journal April 2017
The effective population size of Anopheles gambiae in Kenya: implications for population structure journal March 1998
The Population Genetics of Phytophthora journal April 1997
The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change journal June 2006
A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization journal March 2008
Investigating the causes and consequences of symbiont shuffling in a multi-partner reef coral symbiosis under environmental change journal June 2015
Approximating the coalescent with recombination journal July 2005
Large fluctuations in the effective population size of the malaria mosquito A nopheles gambiae s.s . during vector control cycle journal August 2013
A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host-parasite systems journal September 2008
PSMC analysis of effective population sizes in molecular ecology and its application to black‐and‐white Ficedula flycatchers journal February 2016
Recent Origin of Plasmodium falciparum from a Single Progenitor journal July 2001
The Genome Sequence of the Malaria Mosquito Anopheles gambiae journal October 2002
Early Origin and Recent Expansion of Plasmodium falciparum journal April 2003
A Common Scaling Rule for Abundance, Energetics, and Production of Parasitic and Free-Living Species journal July 2011
Flexibility and Specificity in Coral-Algal Symbiosis: Diversity, Ecology, and Biogeography of Symbiodinium journal November 2003
Origin of the human malaria parasite Plasmodium falciparum in gorillas journal October 2010
Fine-scale population structure and evidence for local adaptation in Australian giant black tiger shrimp (Penaeus monodon) using SNP analysis journal September 2020
Genomic signatures of population decline in the malaria mosquito Anopheles gambiae journal March 2016
Potential Costs of Acclimatization to a Warmer Climate: Growth of a Reef Coral with Heat Tolerant vs. Sensitive Symbiont Types journal May 2010
Data from: Large fluctuations in the effective population size of the malaria mosquito Anopheles gambiae s.s. during vector control cycle dataset January 2013
Genomic signatures of population decline in the malaria mosquito Anopheles gambiae collection January 2016
Supplementary material from "Comparative demography elucidates the longevity of parasitic and symbiotic relationships" collection January 2018