Social parasitism: tricky questions
The various shades of social parasitism in ants have been considered to be among the most intriguing life histories out there. And since long, the study of ant social parasites has been a research field in its own. To summarize progress in this field over the past decade (in which more than half of all papers on this topic were published; Web of Science query), Myrmecological News prepares a Review Article. We believe that despite the large body of literature, important questions will remain unanswered in this review due to a lack of empirical evidence. We thus sounded out current, well-informed opinions on some questions – enjoy!
Flash interviews compiled by Florian M. Steiner
MNB: As far as known, social parasites represent between 1 and 2% of all ant species (all ant species: AntCat; socially parasitic ant species: Buschinger 2009: Myrmecol. News 12: 219-235) – what do you think is the true percentage of ant social parasites out there?
PD: True inter-specific permanent social parasitism (obligatory dulosis, inquilinism), requires high specialization and peculiar adaptations, therefore it is expected to be rare. I agree with the estimate reported in the review by Buschinger and I think that the percentage of these ant social parasites will not change substantially. On the other hand, it is possible, that, with the discovery of new species, a higher percentage of cases of simple temporary parasitism will be detected.
MNB: As far as known, there is a strong imbalance in the geographic distribution of ant social parasites, with temperate regions overrepresented and tropical regions underrepresented – what do you consider as the most likely explanation?
PD: This is one of the important questions waiting for future research efforts. Social parasites are indeed much more frequent in zones with temperate climate and at high elevations. One possible explanation is linked to the evolution of parasitic colony foundation as an adaptation to harsh conditions. When independent colony founding is very risky, due to high queen mortality and/or limitation in nest sites (as occurs in boreal or alpine environment), parasitic colony founding becomes an option. Another factor could be the distribution of host populations, especially for dulotic species which conduct raids. In temperate regions host species may form dense and homogenous populations, which are easier to exploit than those in warm areas, where there is higher species diversity and host nests are dispersed. In tropical regions, it will be easier to find inquilines, which likely evolved via sympatric speciation from (facultatively) polygynous sister species, such as Ectatomma parasiticum from Mexico and Acromyrmex insinuator from Panama.
MNB: How does social parasitism contribute to ant diversification, that is, what would you see as the most common evolutionary routes to social parasitism?
PD: There is more than one evolutionary route to social parasitism. As mentioned above, polygyny involving adoption of young queens in established colonies may lead to inquilinism via sympatric speciation, as suggested by Buschinger already in 1970. For the origin of dulosis, we need the simultaneous evolution of two traits: parasitic colony founding and brood raiding. This is more difficult to explain. There are several hypotheses, starting from the one suggested by Darwin (predation on brood of neighbouring colonies, some of which survived in the parasitic nest), which does not explain parasitic colony founding. It is possible that brood raiding originated from territorial battles including brood robbing and gave rise to dulosis in polygynous species where adoption of young queens occurred. It is interesting to note that dulotic species are typically monogynous.
MNB: What would you see as the three most important research areas in the field of ant social parasitism for the next ten years?
PD: The question of the evolution of social parasitism is exciting and many data are missing on the life history of social parasites, which might shed light on its origin. The mechanisms of chemical integration into host colonies have been explored in very few species, and we are lacking comparative studies. Social parasites are particularly suitable to study the genetic basis for the origin of new phenotypes and phenotypic plasticity.
Alfred Buschinger, Germany
MNB: As far as known, social parasites represent between 1 and 2% of all ant species (all ant species: AntCat; socially parasitic ant species: Buschinger 2009: Myrmecol. News 12: 219-235) – what do you think is the true percentage of ant social parasites out there?
AB: My estimate varies between 4-5% and up to 50%, dependent on the definition of “social parasites”. In a narrow sense, social parasites comprise the permanent inquilines (type Anergates), slave makers (type Polyergus), and temporary social parasites (type Lasius umbratus), including or excluding polygynous species with facultatively parasitic colony foundation and the remaining of mated gynes within the mother nest (type Formica rufa). In a wider sense, the guest ants (type Formicoxenus) may be included, or even so-called “intraspecific social parasites” (e.g., Temnothorax nylanderi). In the widest sense, all facultatively or obligatorily polygynous species could be included where mated offspring queens remain in the mother colony, usurping it like social parasites. However, this behavior also may be interpreted as an extended brood care of the mother colony.
MNB: As far as known, there is a strong imbalance in the geographic distribution of ant social parasites, with temperate regions overrepresented and tropical regions underrepresented – what do you consider as the most likely explanation?
AB: As yet, I don’t see any convincing alternative to my hypothesis that population density of appropriate host species is decisive, particularly for slave-makers, but also for temporary parasites and inquilines. In tropical humid areas, the number of species per area is much higher, but the frequency of the single species is lower (with exceptions, of course).
MNB: How does social parasitism contribute to ant diversification, that is, what would you see as the most common evolutionary routes to social parasitism?
AB: Again, this depends on what we consider as social parasites. Inquilines and slave-makers apparently don’t contribute much to ant diversification; there aren’t many species, although numerous inquilines may still be undiscovered. Temporary social parasites occur in surprisingly high numbers among the genera Lasius and Formica, compared with the total numbers of species in these genera. They all obey Emery’s rule in being closely related to their host species groups. Hence, I still believe in my hypotheses (Buschinger, A., 1990: “Sympatric speciation and radiative evolution of socially parasitic ants – heretic hypotheses and their factual background. – Zeitschrift für Zoologische Systematik und Evolutionsforschung 28: 241-260). Polygynous life habits may be the origin of specialised parasitic behaviors.
In contrast, guest ants (xenobiosis) aren’t closely related to their host species, e.g., myrmicines (Formicoxenus) in nests of Myrmica or Formica spp. and formicines (Polyrhachis) as guests of ponerines (Diacamma, Rhytidoponera). Here, nesting in the vicinity and a mutual tolerance may have been the origin of closer relations (stealing or begging for food from the host species).
MNB: What would you see as the three most important research areas in the field of ant social parasitism for the next ten years?
AB: a) We are in an era in which tropical ant faunas are studied with increasing efforts. I think that intense search for social parasites is recommendable as well as the study of their life histories. However, I understand that this is much more difficult with usually larger colonies as compared with the small colonies of Leptothorax, Temnothorax, Myrmica, Tetramorium, and Plagiolepis species of temperate and cold areas. Many of them can be collected completely, particularly in the cold season when they are concentrated in their nests. Many also can be reared and observed in captivity in small formicaries, which becomes much more difficult with larger colonies
b) It would be desirable to elucidate status and life histories of a few described but extremely rare social parasites, such as parasites of Myrmica (Symbiomyrma and parasitic Myrmica spp.) and Tetramorium spp. (Teleutomyrmex spp.): How do they get into their host colonies? Also, the case of “Myrmica microrubra” appears not to be finally resolved: Is it a bona species? Its behavior is all but typical of a true social parasite. Maybe climatic variations over the course of the year are responsible for the development of two sizes of queens.
c) Finally, an intense search for social parasites in the temperate areas of Asia appears rewarding: The discrepancy between the numbers of known social parasites from the temperate and Mediterranean parts of Europe and from the remainder of Eurasia is as stunning as that between Europe plus North America compared with the humid tropics.
MNB: As far as known, social parasites represent between 1 and 2% of all ant species (all ant species: AntCat; socially parasitic ant species: Buschinger 2009: Myrmecol. News 12: 219-235) – what do you think is the true percentage of ant social parasites out there?
RS: Social parasites continue to be rare. But intensive research in the less studied areas, i.e., in the tropical and subtropical regions, has yielded new species, including new socially parasitic ant species. In the 2010s, at least one new socially parasitic ant species (Myrmicinae) was discovered in the tropics, four (Myrmicinae) in the subtropics and one (Formicinae) in the temperate region. In the future, the number of social parasites will increase, if only efforts are allocated to finding them. However, destruction of natural forests and habitat fragmentation seriously threaten the discovery of new species and their social parasites.
MNB: As far as known, there is a strong imbalance in the geographic distribution of ant social parasites, with temperate regions overrepresented and tropical regions underrepresented – what do you consider as the most likely explanation?
RS: It has remained somewhat of a paradox that cool climates, where the ant faunas are poorest, have many more known social parasites than the warm climates in the tropics and subtropics where the ant faunas are rich. Part of this may result from more research conducted in the cool climates than warm climates over the years, as stated in many reviews (Buschinger 2009: Myrmecol. News 12: 219-235, Hölldobler & Wilson 1990: The ants. Harvard University Press, Cambridge, MA). But there could be some biological explanations, none of which has been tested to my knowledge.
A pattern similar to that of social parasites has been found in the hymenopteran, ichneumonid parasitoids. The diversity of these parasitoids peaks in North America (between 38° and 42°), but the highest diversity of hosts occurs south of North America (Janzen 1981: Ecology 62: 532-537). It is possible that owing to high species richness in the tropics, the populations of the hosts are relatively small or fragmented, and hence difficult for the parasite to locate. In contrast, in the north, many species are common and highly abundant. When the abundance is coupled with highly seasonal reproduction within populations, the parasite may locate potential hosts relatively easily, favouring parasitism in the north.
MNB: How does social parasitism contribute to ant diversification, that is, what would you see as the most common evolutionary routes to social parasitism?
RS: Social parasites of ants are ecologically and behaviourally a diverse group and thus no single process can explain their origin. For many inquilines, a likely scenario for their evolution is within-species parasitism. Within-species parasitism builds on polygyny, a common trait in ants. In a polygynous colony, some queens may start to cheat by producing only sexual and no worker offspring. Hence a chain of events could start, leading to divergence of cheaters and non-cheaters and, eventually, to an inquiline parasite genetically separate from its host.
This is a simplified scenario for the origin of inquilines and thus requires a serious investigation on details of the ecology, behavior and genetics of the inquiline and its host, supplemented with comparative analyses of closely related inquiline-host pairs. Only a thorough investigation could contribute to our understanding of inquiline evolution.
MNB: What would you see as the three most important research areas in the field of ant social parasitism for the next ten years?
RS: More studies (1) on tropical and subtropical ant faunas should contribute to a more balanced view in the geographic distribution of ant social parasites. Still (2) details of the life history and basic ecology of many social parasites are poorly known. (3) Genomic tools offer fruitful prospects for many details of phenotype evolution of inquilines and other social parasites, too.
MNB: As far as known, social parasites represent between 1 and 2% of all ant species (all ant species: AntCat; socially parasitic ant species: Buschinger 2009: Myrmecol. News 12: 219-235) – what do you think is the true percentage of ant social parasites out there?
RMF: Considering my experience with Neotropical ants, I am totally convinced that the percentage of social parasites is considerably higher than 2%. For example, with more than one thousand species described, the genus Pheidole is the most speciose among the myrmicines, and probably among all ants. However, despite the monumental monography by Wilson (2003) on the Pheidole species of the New World, the real diversity of the genus is significantly higher than that currently known, as revealed by recent samplings both in the New World and other regions of the globe. Among the species that remain to be described in this genus, I believe that a significant number will prove to represent social parasites, raising the number of parasites in Pheidole, currently represented by nine species. In addition, several social parasites have been recently discovered among fungus-farming ants (subtribe Attina) and even in turtle ants (genus Cephalotes). It is important to emphasize that a significant number of ants currently described are biologically unknown and may represent parasite forms. Thus, I believe that several new parasite species will become known if we are able to pay more attention to the diversity and natural history of ants, especially in the tropics.
MNB: As far as known, there is a strong imbalance in the geographic distribution of ant social parasites, with temperate regions overrepresented and tropical regions underrepresented – what do you consider as the most likely explanation?
RMF: Although abiotic factors as cooler climate and less intense solar radiation cannot be discarded, I believe that the relatively small number of parasitic species in the tropics may be explained, in part, by a historical trend in the study of ant reproductive biology. Traditionally, studies on the natural history of ants concentrate on species that are easily observable in nature, which establish conspicuous nests and adapt considerably well to the artificial conditions of laboratories. These species generally inhabit physiognomically homogeneous and simple environments. These conditions are more easily found in the temperate biomes of higher latitudes. In the tropics, we have the predominance of dense and highly complex rainforests, with a great part of the ant fauna (up to 70%) restricted to the internal layers of the leaf litter. Thus, it is quite possible that a large number of rarely observed tropical species, whose reproductive biology is unknown, fits into one of the different definitions of social parasites.
MNB: How does social parasitism contribute to ant diversification, that is, what would you see as the most common evolutionary routes to social parasitism?
RMF: In my opinion, ant social parasites’ ability to invade their host nests must have arisen from the sharing of natural microhabitats, communication systems, and chemical mechanisms for nestmate recognition, which is only possible when closely related species are involved. It is corroborated by the usually close phylogenetic relationship between hosts and parasites, both in the “strict” and in a “loose” form of Emery’s rule. This also implies in a sympatric origin of parasitic species, arisen from species subpopulations that concentrate their reproductive efforts on the production of sexual offspring, and gradually become genetically distinct and reproductively isolated from their future hosts (strict Emery’s rule). Later, both the parasite and the host experience further evolution and isolation, which could explain the cases of host shift and the exploitation of several hosts by the same parasite species (loose Emery’s rule). Our knowledge about the selective forces behind the evolutionary routes to social parasitism is still incipient, but the difficulties faced by solitary queens when founding their colonies must play an important role in this process.
MNB: What would you see as the three most important research areas in the field of ant social parasitism for the next ten years?
RMF: I would say that myrmecologists must invest in the study of the reproductive biology of tropical ants, both in the field and lab conditions, since the gap in our knowledge about the natural history of ants in these regions may be related to some extent to the imbalance in the geographic distribution of ant social parasites. Second, studies on social parasitism should consider a closer relationship with comprehensive phylogenetic frameworks for ants. Tracing the independent origins of social parasites in the ant tree of life would be the first step to answer the questions related to the presence of a higher number of parasite species in certain ant genera or subfamilies. Finally, myrmecologists could apply some of the recent and advanced morphological tools, including cybertaxonomic technology, to understand the evolution of the morphological syndromes related to parasitic habits. In fact, these tools could lead to the recognition of potentially parasitic species based on proportions between structures and details of the external and internal anatomy of individuals. This would greatly add to our knowledge about the evolution of the social parasitism in ants.
MNB: As far as known, social parasites represent between 1 and 2% of all ant species (all ant species: AntCat; socially parasitic ant species: Buschinger 2009: Myrmecol. News 12: 219-235) – what do you think is the true percentage of ant social parasites out there?
SF: In some of the well-studied faunas, the percentage of social parasites is much higher, such as in Switzerland, where up to 30% of all species are at least temporarily parasitic. I think we might still miss many workerless inquilines, especially of host species with large colonies as the queens are not easy to find and inquilines tend to be rare. This is particularly true for tropical, arboreal species, which are difficult to study.
MNB: As far as known, there is a strong imbalance in the geographic distribution of ant social parasites, with temperate regions overrepresented and tropical regions underrepresented – what do you consider as the most likely explanation?
SF: Slavemaking ants appear to be more common in temperate to boreal climates, where host communities are composed of very few species with an extremely high density of colonies, such as Temnothorax, Leptothorax or Formica populations. This is required if a slavemaker has to raid multiple host colonies in the vicinity. Also for slavemakers, new species are still described; for example; we described a new slavemaker species, just 5 years ago from the US (Seifert et al. 2014: ZooKeys 368: 65-77). There might also be lots of slavemakers in boreal regions, such as Siberia, China etc., which are not well studied to this point. In the tropics, I am sure we miss many inquilines, which are not easy to detect. As many ants are only known from workers falling into traps, which will not happen with workerless inquilines, I am sure the percentage of parasitic species will go up.
MNB: How does social parasitism contribute to ant diversification, that is, what would you see as the most common evolutionary routes to social parasitism?
SF: Social parasites are most likely to arise either in sympatry or allopatry from a non-parasitic ancestor, which serves often as the first host. social parasitism does thus contribute to species richness in the ants. On the other hand, when only a few % of all ants are parasitic, their contribution is rather minor, or?
MNB: What would you see as the three most important research areas in the field of ant social parasitism for the next ten years?
SF: I think we will make significant progress on the genes underlying parasitic behaviors using transcriptomics and genomics, we will see which genes or gene families are lost or multiplied. We will get a better understanding of the coevolution between social parasites, both on a behavioral, chemical, and molecular level. We can identify genes under selection in both parasites and hosts. And then there are still lots of unexpected natural history discoveries awaiting us, tricks of manipulative parasites and evolution of host defenses.
At the begining place a seemingly misplaced sentence that is understandable only after you have read the last lines: It is beyond my physical power and nervous resilience to write some 15 publications a year in a scientific world where you have to communicate with stupid automates instead of human beings when submitting a manuscript or where have to pay some 700 € to have finally published a small five-page article.
The blog speculates on the share of socially parasitic ant species within the total species number. We have very precise numbers for a region of some 2 million square kilometers. It is by far the best investigated area of the world both in terms of ant taxonomy and ant biology. No landslides regarding species-level taxonomy are expectable here thanks to a very thorough NUMOBAT investigation performed now over nearly 40 years. This region is part of the submediterranean, temperate, subboreal and boreal zones of the Palaearctic and as such it may be considered as representative for the largest zoogeographic region of the world. Socially parasitic species make up here 30% of the total – within that 17.2% temporary social parasites, 8.9% inquilines and 3.9% obligatory dulotic species. These data are presented in few sentences in Seifert (2018) on the pages 27-28 and 61. I wrote this book also under the bleak awareness, (or in despair) that I will not succeed, in the life time remaining, to have published significant results in the usual form – in a series of isolated scientific papers with attractive or alerting titles. Accordingly, in order to get some psychological relief from this threatening castration, I tried to include all this information in a very brief, condensed form within a book the size of which was definitely aimed to remain below the caliber to make it usable in defense against a burglar. There is plenty of such material – usually based on sufficient evidence. One example are six sentences hidden in the right column on page 144 – very clear results on global warming and ant phenology which are in line with data on bird arrival dates or vascular plant phenology. I encourage not only to browse this book diagonally with short looks on some attractive photos but to really r–e–a–d it consciously. I was embarrassed by a naive reviewer who classified this book as belonging to the category of “field guides”.
As for socially parasitic ants in the tropics, it is clear for me that a lot of further inquilines will be discovered but it is also clear for me that, even after a thorough investigation, the percentage of temporary social parasites and dulotic species will stay much below the figures evident for the Palaearctic. This disparity is real and we know many of the reasons.
If you intend to respond to this contribution, please, do it by e-mail. I do not check blogs and refuse to participate in Twitter Facebook and other asocial media.
Bernhard Seifert
Seifert, B 2018: The Ants of Central and North Europe. – Lutra VerlagTauer, 412 pp.
Yes, I’m totaly convinsed that Seifert is a great myrmecologist and that his book is very important! And that his persentage of 30 % socially parasitic species is correct.
Great work, Seifert! Carry on!!!
For those 30 % you can go back to Heinrich Kutter. In his 1969 booklet he already postulated the occurrence of parasitic ants and found (on figures from his own country!) a percentage of 30 % parasitic ants in Switzerland. So good is that estimate that Seifert mentions the same figure based on a much grander area. Good…..
And in his 1968 list of parasitic ants of the world H. Kutter gave a fig. of 31 % for Switzerland.