Cryptic Species, Agriculture, and Confirmation Bias
Posted by Andrew McGuire | May 31, 2018
Imagine this. You are an avid fisherman in south-eastern Australia. You relish getting away to the many lakes in the nearby mountains. Each lake is a bit different, different surroundings, different fishing holes, but you always see the same minnows, or perhaps two species as you heard a ranger say at a campfire talk, “based on expert taxonomic assessment.” You call them brown minnows, some call them mountain galaxias. They seem common, normal; but we see not as a minnow sees, but with human eyes and thoughts.
In 2012, a group of Aussie scientists (Adams et al. 2014) made a discovery: the minnows from the different lakes that look the same to you, are actually 15 distinct species. What was thought to be one or two species before, even by simple DNA tests, became 15 species with more comprehensive genetic testing (“involving multi-locus nDNA markers”). Organisms such as these minnows, which look very similar, even identical by most standards, but are different species are called cryptic species. A group of these is called a cryptic complex of species. Because of the high number of minnow species, this case is raised to the “hyper-cryptic complex” status.
It turns out these cryptic complexes, groups of “taxonomically confused species,” (taxonomy is the classification based on physical differences) are found all around the world and among all major organism types. They are common in protozoa and fungi, insects and nematodes, and even mammals. Because they are so common, it has caused science to delve deeper into the differences between species, and how to tell them apart. Cryptic species are true species, not biotypes or sub-species. So, just what is a species?
What is a species?
Species are the basic units of biology. However, distinguishing one species from another is not always easy. The basic limitation between species is that they cannot produce offspring, so scientists have traditionally relied on close observation of reproductive success between visually similar organisms, but even with large, easy-to-see mammals, the differences are not always plain. In 2001, using genetic evidence, the African elephant was found to be two, cryptic, species, the forest and savannah elephants (Roca et al. 2001). I remember as a kid seeing an enraged elephant in the San Diego zoo. Now I wonder if it was a forest elephant in a faux-savannah enclosure…
In uncontrolled environments, or with microscopic or rare organisms, or those that reproduce asexually, the observation of reproductive success or failure may be impossible. Furthermore, many cryptic species have “non-visual mating habits” that are not easy to detect but which keep them “reproductively isolated” from other similar organisms. The species themselves are diverse, with different life cycles, feeding preferences, pheromones, environmental tolerances, all cryptic to our senses. Although in the case of elephants, the two cryptic species live in different habitats, that is not always the case. Some live in the same location, side-by-side, further complicating their identification.
How are cryptic species found?
The problems in species identification are serious; there is even a 2013 paper titled How to Fail at Species Delimitation (Carstens et al. 2013). However, the recent development of extensive DNA or other genetic testing has allowed an exponential increase in the identification of cryptic species (Shneyer and Kotseruba, 2015). It seems now that wherever taxonomists probe with the new tests, they find new species, including eight species of zebra. Some researchers say that the data suggests that number of species should at least be doubled. The famed minnow discoverers, Adams et al., even suggest that hyper-cryptic species complexes are “likely to be extremely common in those groups that make up the base of the pyramid of planetary biodiversity,” that rather than rare occurrences, they may be “the tip of the taxonomic iceberg.”
While all this is important for species conservation, as with the elephants, and for maintaining scientific inquiry, it is also relevant for agriculture.
In the soil
The soil is still relatively unexplored when it comes to species, but even where species have been studied there may be many cryptic species. In plant parasitic nematodes, “the possibility of undescribed or mis-described species is very high” and many have been found in free-living nematodes (Palomares-Rius et al., 2014). The same has been surmised for fungi and algae. Soil organisms are difficult to study; the existence of cryptic species just adds another layer of complexity.
Crops and weeds
The case for cryptic species in plants is not clear. Because of their genetics, the molecular methods that work in animals are not reliable in plants (Shneyer and Kotseruba, 2015). Therefore, there are not many cases of cryptic plant species reported. However, Shneyer and Kotseruba believe that as methods improve, and more plants are examined, this number will increase to levels similar to other organism groups. For example, cryptic species in plants are now being discovered using nuclear ribosomal DNA sequencing (Okuyama and Kato, 2009). The intensively studied grass Brachypodium distachyon, a model grass for cereals, was eventually found to be three species (Catalán et al., 2012). In weeds, Hrusa and Gaskin (2008) discovered a new species of Russian thistle hidden in the invasive population in California.
As with other organisms, differences in plant cryptic species can be subtle to our senses. Cryptic plant species can differ in the types of secondary metabolites they produce. This can affect pests and disease susceptibility, stress tolerance, interactions with soil microbes, and palatability to herbivores. Flowering plants that are pollinated by insects and birds may look alike, but may differ in their scents, leading to differences in pollinators. Evidence also points to differences in “…development, photosynthesis, and in ecological niches” (Shneyer and Kotseruba 2015).
Insects, generalists, and biocontrol
Cryptic species are common in insects, including those important to agriculture. Insect cryptic species can differ in the plants that they are associated with, or in the case of parasitoids, with their insect hosts (Walter 2005). We call species that live on and eat a variety of plants generalist species. However, researchers using new tests have found that some so-called generalist species are groups of cryptic species. For example, most generalist parasitoids of aphids are now thought to be cryptic species complexes (Derocles et al., 2016), each species parasitizing a specific species of aphid.
The basic assumption of modern pest control tactics is that we understand the target organism, the details of its life cycle, its preferred habitat and food, etc. Both biocontrol, and to a lesser extent, control with pesticides rely on this detailed information. The presence of an unknown cryptic species, either in the pest population, or in the biocontrol agent population, can cause control efforts to fail for no apparent reason (Walter 2005). This is because distinct species react differently to control methods, whether cultural, biocontrol, or pesticides. Examples where misidentification of a cryptic species complex as one species has thwarted biological control efforts are found both in insects (citrus red scale in California) and weeds (Salvania in Australia).
Cryptic species complicate agricultural research, especially related to pest control. A pest species that has not been confirmed to be just one species through genetic testing is only a hypothesis, one that could quickly be overturned; given recent findings, one might say likely to be overturned. If that one species turns out to be a cryptic species complex, each with subtle but crucial differences, the problems of finding a control method, especially a biocontrol method, can expand quickly beyond the time and resources of a single species project.
Past confirmation bias
The term “cryptic species” first appeared in 1940 – it is not a new discovery – which reveals a peril of scientific inquiry; we tend to see only that which confirms what we expect to see. With cryptic species, this confirmation bias is revealed in hindsight; once cryptic species are discovered, then experts are often able to distinguish between the newly discovered species using visible external or internal differences (Medina et al., 2012). Scientists who had believed they were looking at one species either ignored the differences or explained them as variation within the species.
Cryptic species are a good reminder of our species’ foibles, that we should not always trust what we see. Perhaps the contradictory Russian proverb can guide us, “Trust, but verify.” We cannot progress without trusting past scientific observations, but given our knowledge of cryptic species, we should only assume we are dealing with one species if it has been verified with genetic tools. Rather than ignoring observed differences between individuals of an assumed species, we should use the available tools to verify if the anomaly is an error in our own observations, or those of past research.
Adams, Mark, Tarmo A. Raadik, Christopher P. Burridge, and Arthur Georges. 2014. “Global Biodiversity Assessment and Hyper-Cryptic Species Complexes: More Than One Species of Elephant in the Room?” Systematic Biology 63 (4): 518–33. https://doi.org/10.1093/sysbio/syu017.
Carstens, Bryan C., Tara A. Pelletier, Noah M. Reid, and Jordan D. Satler. 2013. “How to Fail at Species Delimitation.” Molecular Ecology 22 (17): 4369–83. https://doi.org/10.1111/mec.12413.
Catalán, Pilar, Jochen Müller, Robert Hasterok, Glyn Jenkins, Luis A. J. Mur, Tim Langdon, Alexander Betekhtin, Dorota Siwinska, Manuel Pimentel, and Diana López-Alvarez. 2012. “Evolution and Taxonomic Split of the Model Grass Brachypodium Distachyon.” Annals of Botany 109 (2): 385–405. https://doi.org/10.1093/aob/mcr294.
Derocles, Stephane a. P., Manuel Plantegenest, Jean-Yves Rasplus, Alexia Marie, Darren M. Evans, David H. Lunt, and Anne Le Ralec. 2016. “Are Generalist Aphidiinae (Hym. Braconidae) Mostly Cryptic Species Complexes?” Systematic Entomology 41 (2): 379–91. https://doi.org/10.1111/syen.12160.
Hrusa, G. F., and J. F. Gaskin. 2008. “The Salsola Tragus Complex in California (Chenopodiaceae): Characterization and Status of Salsola Australis and the Autochthonous Allopolyploid Salsola Ryanii Sp. Nov.” Madroño 55 (2): 113–131.
Liu, Shu-sheng, John Colvin, and Paul J De Barro. 2012. “Species Concepts as Applied to the Whitefly Bemisia Tabaci Systematics: How Many Species Are There?” Journal of Integrative Agriculture 11 (2): 176–86. https://doi.org/10.1016/S2095-3119(12)60002-1.
Martin, Robert D. 2012. “Primates.” Current Biology 22 (18): R785–90. https://doi.org/10.1016/j.cub.2012.07.015.
Medina, Rafael, Francisco Lara, Bernard Goffinet, Ricardo Garilleti, and Vicente Mazimpaka. 2012. “Integrative Taxonomy Successfully Resolves the Pseudo-Cryptic Complex of the Disjunct Epiphytic Moss Orthotrichum Consimile s.l. (Orthotrichaceae).” Taxon 61 (6): 1180–98.
Okuyama, Yudai, and Makoto Kato. 2009. “Unveiling Cryptic Species Diversity of Flowering Plants: Successful Biological Species Identification of Asian Mitellausing Nuclear Ribosomal DNA Sequences.” BMC Evolutionary Biology 9 (May): 105. https://doi.org/10.1186/1471-2148-9-105.
Palomares-Rius, Juan E., Carolina Cantalapiedra-Navarrete, and Pablo Castillo. 2014. “Cryptic Species in Plant-Parasitic Nematodes.” Nematology 16 (10): 1105–18. https://doi.org/10.1163/15685411-00002831.
Roca, Alfred L., Nicholas Georgiadis, Jill Pecon-Slattery, and Stephen J. O’Brien. 2001. “Genetic Evidence for Two Species of Elephant in Africa.” Science 293 (5534): 1473–77. https://doi.org/10.1126/science.1059936.
Shneyer, V. S., and V. V. Kotseruba. 2015. “Cryptic Species in Plants and Their Detection by Genetic Differentiation between Populations.” Russian Journal of Genetics: Applied Research 5 (5): 528–41. https://doi.org/10.1134/S2079059715050111.
Walter, G. H. 2005. Insect Pest Management and Ecological Research. Cambridge University Press.