UniqueparasiteaDNAinmoacoprolitesfromNew COMMENTARY ... · Zealandia food web. In this enhanced...
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COMMENTARY Unique parasite aDNA in moa coprolites from New Zealand suggests mass parasite extinctions followed human-induced megafauna extinctions Kevin D. Lafferty a,1 and Skylar R. Hopkins b Having split early from Gondwana, Zealandia (now modern New Zealand) escaped discovery until the late 13th century, and therefore remains an important glimpse into a human-free world. Without humans or other land mammals, diverse and peculiar birds evolved in isolation, including several flightless moa species, the giant pouakai eagle ( Harpagornis moorei ), the kiwi (Apteryx mantelli ), and the kakapo parrot (Strigops habroptila). This unique community has fascinated paleoecologists, who have spent almost two centuries devising new ways to glean information from ancient bird remains. In PNAS, Boast et al. (1) apply one recent technological advance, ancient DNA (aDNA) metabarcoding, to confirm previous discoveries and re- port new details about moa and kakapo diets, parasites, and niches. Their efforts confirm Zealandia was a lot dif- ferent before humans arrived. Zealandia’s most diverse avian oddities were the moa. Moa research goes back to the early 1800s, when the M aori told legends to colonizing Europeans about giant birds and showed them fossilized moa bones in caves. Those fossils belonged to at least nine moa species ranging from 1 to 4 m tall, some with notable sexual dimorphism (2). The moa species have different fossil distributions, morphology, and gizzard contents, suggesting they partitioned Zealandia’s re- sources into distinct ecological niches. To better under- stand how moas coexisted and interacted with other species, paleontologists have turned to another abun- dant deposit that moas left behind: coprolites (fossilized dung). The 2,000 moa coprolites that have been col- lected thus far contain plants, fungi, microbes, and in- testinal parasites (3), a priceless resource for creating ecological snapshots from Zealandia. Until the aDNA revolution, however, these snapshots were blurry (4). Sequencing aDNA allows paleontologists to iden- tify dung-encased organisms at finer resolution than they see with a microscope. Studying aDNA is nerve- wracking, because it degrades over time and each sample can become contaminated where it lies or during sample handling, transport, and storage. How- ever, dedicated aDNA facilities and rigorous protocols help reduce contamination (5). Even then, authentic aDNA fragments can be hard to decipher, because short diagnostic DNA barcodes are still unavailable for most plants and animal species (1). Thus, scientists who work with aDNA need to be careful, both in their techniques and their interpretation. When it works, the effort pays off with insights not imaginable when pa- leontologists cracked open that first moa coprolite. Boast’s research group has been around the aDNA block before, having used first-generation sequencing techniques on plant, microbe, and parasite aDNA from moa coprolites to yield family- and even genus- level taxonomic resolution for several taxa that the moa interacted with (6, 7). However, first-generation techniques are too time-consuming and expensive for compiling a comprehensive ancient food web. To make the most from their samples, Boast et al. (1) switched to high-throughput sequencing, which con- firmed previous first-generation results and unearthed several hitherto unknown ecological interactions be- tween the moa and plants, fungi, and parasites. In addition to describing these new results, Boast et al. (1) synthesize past findings to add resolution to the Zealandia food web. In this enhanced snapshot from Zealandia (Fig. 1), an upland moa (Megalapteryx didiformis) stops to eat moss under a southern-beech tree (Nothofagaceae) and then defecates feces laced with parasite eggs on the forest floor. As with many other upland moa, it acquired parasitic trematodes when feeding at a small alpine pond and heterakoid nematodes when eating contaminated ferns and other vegetation. How- ever, the moa’s real concern is the pouakai, the world’s largest eagle and the only moa predator. A nearby South Island giant moa (Dinornis robustis) has no interest in the upland moa’s moss. Instead, it lunges a US Geological Survey, Western Ecological Research Center, c/o Marine Science Institute, University of California, Santa Barbara, CA 93106; and b National Center for Ecological Analysis and Synthesis, Santa Barbara, CA 93101-5504 Author contributions: K.D.L. designed research; K.D.L. and S.R.H. performed research; S.R.H. analyzed data; and K.D.L. and S.R.H. wrote the paper. The authors declare no conflict of interest. Published under the PNAS license. See companion article on page 1546. 1 To whom correspondence should be addressed. Email: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1722598115 PNAS | February 13, 2018 | vol. 115 | no. 7 | 1411–1413 COMMENTARY Downloaded by guest on December 24, 2020
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COMMENTARY
Unique parasite aDNA in moa coprolites from NewZealandsuggestsmassparasiteextinctionsfollowedhuman-inducedmegafauna extinctionsKevin D. Laffertya,1 and Skylar R. Hopkinsb
Having split early from Gondwana, Zealandia (nowmodern New Zealand) escaped discovery until the late13th century, and therefore remains an importantglimpse into a human-free world. Without humansor other land mammals, diverse and peculiar birdsevolved in isolation, including several flightless moaspecies, the giant pouakai eagle (Harpagornismoorei), the kiwi (Apteryx mantelli ), and the kakapoparrot (Strigops habroptila). This unique communityhas fascinated paleoecologists, who have spent almosttwo centuries devising new ways to glean informationfrom ancient bird remains. In PNAS, Boast et al. (1) applyone recent technological advance, ancient DNA (aDNA)metabarcoding, to confirm previous discoveries and re-port new details about moa and kakapo diets, parasites,and niches. Their efforts confirm Zealandia was a lot dif-ferent before humans arrived.
Zealandia’s most diverse avian oddities were themoa. Moa research goes back to the early 1800s,when the M�aori told legends to colonizing Europeansabout giant birds and showed them fossilized moabones in caves. Those fossils belonged to at least ninemoa species ranging from 1 to 4 m tall, some withnotable sexual dimorphism (2). The moa species havedifferent fossil distributions, morphology, and gizzardcontents, suggesting they partitioned Zealandia’s re-sources into distinct ecological niches. To better under-stand how moas coexisted and interacted with otherspecies, paleontologists have turned to another abun-dant deposit that moas left behind: coprolites (fossilizeddung). The 2,000 moa coprolites that have been col-lected thus far contain plants, fungi, microbes, and in-testinal parasites (3), a priceless resource for creatingecological snapshots from Zealandia. Until the aDNArevolution, however, these snapshots were blurry (4).
Sequencing aDNA allows paleontologists to iden-tify dung-encased organisms at finer resolution thanthey see with a microscope. Studying aDNA is nerve-wracking, because it degrades over time and each
sample can become contaminated where it lies orduring sample handling, transport, and storage. How-ever, dedicated aDNA facilities and rigorous protocolshelp reduce contamination (5). Even then, authenticaDNA fragments can be hard to decipher, becauseshort diagnostic DNA barcodes are still unavailablefor most plants and animal species (1). Thus, scientistswho work with aDNA need to be careful, both in theirtechniques and their interpretation. When it works, theeffort pays off with insights not imaginable when pa-leontologists cracked open that first moa coprolite.
Boast’s research group has been around the aDNAblock before, having used first-generation sequencingtechniques on plant, microbe, and parasite aDNAfrom moa coprolites to yield family- and even genus-level taxonomic resolution for several taxa that themoa interacted with (6, 7). However, first-generationtechniques are too time-consuming and expensive forcompiling a comprehensive ancient food web. Tomake the most from their samples, Boast et al. (1)switched to high-throughput sequencing, which con-firmed previous first-generation results and unearthedseveral hitherto unknown ecological interactions be-tween the moa and plants, fungi, and parasites. Inaddition to describing these new results, Boast et al.(1) synthesize past findings to add resolution to theZealandia food web.
In this enhanced snapshot from Zealandia (Fig. 1),an upland moa (Megalapteryx didiformis) stops to eatmoss under a southern-beech tree (Nothofagaceae)and then defecates feces laced with parasite eggson the forest floor. As with many other upland moa,it acquired parasitic trematodes when feeding at asmall alpine pond and heterakoid nematodes wheneating contaminated ferns and other vegetation. How-ever, the moa’s real concern is the pouakai, theworld’s largest eagle and the only moa predator. Anearby South Island giant moa (Dinornis robustis) hasno interest in the upland moa’s moss. Instead, it lunges
aUS Geological Survey, Western Ecological Research Center, c/o Marine Science Institute, University of California, Santa Barbara, CA 93106;and bNational Center for Ecological Analysis and Synthesis, Santa Barbara, CA 93101-5504Author contributions: K.D.L. designed research; K.D.L. and S.R.H. performed research; S.R.H. analyzed data; and K.D.L. and S.R.H. wrote the paper.The authors declare no conflict of interest.Published under the PNAS license.See companion article on page 1546.1To whom correspondence should be addressed. Email: [email protected].
www.pnas.org/cgi/doi/10.1073/pnas.1722598115 PNAS | February 13, 2018 | vol. 115 | no. 7 | 1411–1413
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forward and snaps up a tasty-looking mushroom near a southern-beech trunk. It is lucky to have found this gem, because kakaposand upland moas also seek out Cortinariusmushrooms. The fungalspores will pass through the giant moa’s digestive system, in whichlive apicomplexan parasite oocysts (Eimeriidae) and an ascaridnematode or two. Later, defecated fungal spores will have thechance to establish a mycorrhizal relationship with a new host tree,and a kiwi might accidentally eat the defecated oocysts. Ancientparadise, it turns out, had abundant dung and parasites.
Such interactions continued within this robust Zealandiaecosystem, despite environmental and climate fluctuations (8,9), until the first M�aori landed their canoes on Zealandia and
named it Aotearoa. TheM�aori hunted themoa, which had only fearedthe pouakai, anddrove the ninemoa species extinct within∼200 y (10).
Boast et al. (1) show that some species that interacted with themoa survived their loss. For instance, the upland moa’s Eimeriidcoccidians still parasitize extant kiwi. Likewise, animal-dispersedmycorrhizal fungi still exist in New Zealand’s modern forests evenwithout extant animal dispersers (11). These fungi might be eco-logical anachronisms, like the giant fruits in the Americas that rotunder their trees without extinct mammalian megafauna to eatthem and disperse their seeds (12). Just as the long-lived treesin the Americas have slowly declined without their ancient seeddispersers, so too might the moa-dispersed fungi and their
Fig. 1. The ancient Zealandia food web was much different from that in present-day New Zealand, and it included several ecological interactionsthat Boast et al. (1) revealed by sequencing aDNA frommoa coprolites. For instance, the upland moa (M. didiformis) ate moss, ferns, mycorrhizalfungi that require animal-assisted dispersal, and aquatic vegetation. The upland moa also accidentally ate (and was infected by) aquatictrematode larvae (Notocotylidae) and apicomplexan parasites (Eimeriidae), which still exist in extant kiwi. Other parasites that once infectedmoas, like several heterakoid nematode species, have not been seen since the moa extinctions. Dashed arrows indicate interactions lost since themoa extinctions.
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southern-beech tree hosts decline unless they adapt to use newspore dispersers or moa deextinction ideas become reality (13).
Other species were not robust.Withoutmoa, the pouakai starved.Pouakai is the most obvious secondary extinction to follow the moa,but Boast et al. (1) suggest that other species fell like a teeteringJenga tower after a critical piece is pulled. In particular, several heter-akoid nematode species had coevolved to specialize on moa, andhave not been seen since the moa disappeared. Other moa andpouakai parasites (most likely several never-seen, host-specific lice)were probably lost. These secondary extinctions result becausecoevolved complex systems cannot evolve robustness to swift, un-predictable events like the M�aori’s arrival and rapid domination (14).How many secondary extirpations or extinctions occurred is not yetclear, and will remain unknown until there are larger sequence librar-ies from extant species that can be used to confirm their absences. Tounderstand the past with aDNA, onemust also sequence the present.
Between the ancient moa extinctions and the present, Euro-peans and their introductions further altered New Zealand’s bio-diversity. Winners included weeds, pests, and people. Theirparasites were winners too. On the other hand, specialist para-sites, particularly those with complex life cycles, should be leastrobust to secondary extinction (15) and should go down with theship. To that end, parasite extinctions have continued in NewZealand. In 1904, scientists discovered the kakapo tapewormStringopotaenia psittacea (16), which has not been seen sincethe kakapo’s dramatic decline toward near extinction. Soon after,
a chewing louse (Huiacola extinctus) went extinct (17), along withits host, the huia (a wattlebird hunted for its feathers). More re-cently, the louse Rallicola (Aptericola) pilgrimi was lost after itshost, the smallest kiwi (Apteryx owenii ), was translocated topredator-free islands (18). Therefore, most New Zealand extinc-tions have probably been parasite extinctions.
Society will decide whether we preserve, ignore, or extirpatespecies we find insignificant, threatening, or disgusting. Somepoint out that parasites deserve protection because they canplay important roles as consumer species (19). Others considerthat ignoring these associated species is taxonomic chauvinism(20); it is like counting sunken ships in a naval battle, withoutmourning the sailors that go down with those ships. The extentto which we value host vessels or their parasite passengers ismost often answered by veterinarians. When veterinarians treatedthe last remaining California condors in 1987, they found thecondor louse, Colpocephalum californici, a symbiont whose an-cestors had flown with condors over plains populated by mam-moths and saber-toothed tigers; they then exiled the condorlouse to extinction with an insecticide treatment (20). Had moasurvived to face Europeans, New Zealand veterinarians wouldhave likely done the same to moa parasites.
AcknowledgmentsAny use of trade, product, or firm names in this publication is for descriptivepurposes only and does not imply endorsement by the US Government.
1 Boast AP, et al. (2018) Coprolites reveal ecological interactions lost with the extinction of New Zealand birds. Proc Natl Acad Sci USA 115:1546–1551.2 Worthy TH, Scofield RP (2012) Twenty-first century advances in knowledge of the biology of moa (Aves: Dinornithiformes): A new morphological analysis and moadiagnoses revised. N Z J Zool 39:87–153.
3 Wood JR, Wilmshurst JM (2014) Late Quaternary terrestrial vertebrate coprolites from New Zealand. Quat Sci Rev 98:33–44.4 Cole TL, Wood JR (2017) The ancient DNA revolution: The latest era in unearthing New Zealand’s faunal history. N Z J Zool 44:1–30.5 Cooper A, Poinar HN (2000) Ancient DNA: Do it right or not at all. Science 289:1139.6 Wood JR, et al. (2013) A megafauna’s microfauna: Gastrointestinal parasites of New Zealand’s extinct moa (Aves: Dinornithiformes). PLoS One 8:e57315.7 Wood JR, et al. (2013) Resolving lost herbivore community structure using coprolites of four sympatric moa species (Aves: Dinornithiformes). Proc Natl Acad SciUSA 110:16910–16915.
8 Rawlence NJ, et al. (2012) The effect of climate and environmental change on the megafaunal moa of New Zealand in the absence of humans. Quat Sci Rev50:141–153.
9 Allentoft ME, et al. (2014) Extinct New Zealand megafauna were not in decline before human colonization. Proc Natl Acad Sci USA 111:4922–4927.10 Perry GLW, Wheeler AB, Wood JR, Wilmshurst JM (2014) A high-precision chronology for the rapid extinction of New Zealand moa (Aves, Dinornithiformes).Quat
Sci Rev 105:126–135.11 Wood JR, et al. (2015) Novel interactions between non-native mammals and fungi facilitate establishment of invasive pines. J Ecol 103:121–129.12 Janzen DH, Martin PS (1982) Neotropical anachronisms: The fruits the gomphotheres ate. Science 215:19–27.13 Wood JR, Perry GLW, Wilmshurst JM (2017) Using palaeoecology to determine baseline ecological requirements and interaction networks for de-extinction
candidate species. Funct Ecol 31:1012–1020.14 Strona G, Lafferty KD (2016) Environmental change makes robust ecological networks fragile. Nat Commun 7:12462.15 Lafferty KD (2012) Biodiversity loss decreases parasite diversity: Theory and patterns. Philos Trans R Soc Lond B Biol Sci 367:2814–2827.16 Beveridge I (1978) A Taxonomic Revision of the Genera Cittotaenia Riehm, 1881, Ctenotaenia, Railliet, 1893, Mosgovoyia Spasskii 1951 and Pseudocittotaenia
Tenora, 1976: Cestoda, Anoplocephalidae (Editions de Museum, Paris).17 Mey E (1990) Eine neue ausgestorbene vogel-Ischnozere von neuseeland, Huiacola extinctus (Insecta, Phthiraptera). Zool Anz 224:49–73. German.18 Buckley TR, et al. (2012) The conservation status of small or less well known groups of New Zealand terrestrial invertebrates. N Z Entomol 35:137–143.19 Dougherty ER, et al. (2016) Paradigms for parasite conservation. Conserv Biol 30:724–733.20 Pizzi R (2009) Veterinarians and taxonomic chauvinism: The dilemma of parasite conservation. J Exot Pet Med 18:279–282.
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