Invasive species

The story of colonizing species encompasses a wide range of "colonizing ability". From attempts at deliberate introductions, we know that some species just don't have a great potential to colonizing new territory; others succeed for a while and then explode.

We don't know the number of failed accidental introductions, but we do know a lot about one extreme -- the accidental introductions of alien species that become invasive problems. Such species have such a high colonizing potential (at least in certain contexts) that their populations explode beyond the numbers in their native ranges.

Brown (1957), discussing the colonizing ability of populations at the center of population ranges, brings in a number of examples of such invasive species, whose spread is often apparent within the span of decades or even years. One of these is the invasion and spread of the fire ant into North America.

Fire ants were inadvertently imported to the U.S. from South America sometime around 1918. Wilson (1953) gave an account of the early population history of these ants. It was clear in these early years that there were two forms of the ants, a dark-colored form and a red form. Of these, the red form was the more invasive, but it appeared that the real invasive character of the population might be attibutable to hybridization between the two. Brown (1957:259) quoted Wilson (1953):

For about ten years [the Mobile population] remained both genetically homogeneous, corresponding to the dark southern race richteri Forel of the South American parental population, and relatively unsuccessful in its new surroundings. In the period following 1930 a smaller reddish form rose to abundance, interbred extensively with the original dark form, and apparently precipitated the species' explosive increase to pest proportions. By 1949 the reddish form had largely replaced the dark form, which had become limited principally to the southern strip of the main population and part of its eastern and western periphery and to two outlying, isolated populations in Mississippi.

To this, Brown (1957:260) added:

The dark-phase colonies are now limited to certain separated peripheral areas of the range and a few minor enclaves within the main area of infestation, and even where they occur, they are often in the minority. All degrees of intergration [sic] link dark and red phases. As the red forms press outward, the dark forms apparently suffer both genetic swamping and competition-aggression, and consequently tend to extinction in most habitats. In spite of these forces at work against it, the dark form persists, genetically embedded, so to speak, in the dense and expanding matrix of red populations. This case is very instructive in showing how, regardless of its origin in this particular case, a genetic change actually spreads from a central point of introduction and tends in this way to cause a central-peripheral differential.

For Brown, the entire case of fire ant invasion is an evidence for central species having a greater colonizing potential than peripheral ones, because the tropical Solenopsis species were displacing congeneric S. geminata and S. xyloni, which had been common throughout the Caribbean and Gulf of Mexico coastal areas. The entire New World, from the point of view of Solenopsis is a zone with a tropical center and subtropical and temperate peripheries. In this case, Brown proposed that the displacement of fire ants from a central area (southern Brazil or Argentina) to the northern periphery had enabled the invasive character of the spread, although with probable adaptive changes in the new colonizing population.

The other element of this argument is that populations face more competition from similar competitor species and more natural disease and predation in the central parts of their ranges. Where a species can exist at higher densities, it can support more parasites, pathogens, and predators. For fire ants, these predators and parasites include a number of species that have been deliberately introduced as part of efforts to control their spread in the U.S.

Fire ant initial invasion area from 1928-1949

Fire ant dispersal in southern U.S. from ca. 1939 to 1995. Figure from Brown 1957 p. 260. Brown took the plot from Wilson (1951).

I looked at that figure and gasped -- imagine living in one of the outlying counties in 1949 and knowing that pattern of spread.

Of course, from there the dispersal simply exploded. A good review of the history of fire ant spread was given by Anne-Marie Callcott and Homer Collins (1996). Their maps of infested counties over time say it all:

Fire ant dispersal map, 1939-1995

Fire ant dispersal in southern U.S. from ca. 1939 to 1995. Figures from Callcott and Collins 1996, pp. 244-246, recompiled for web format.

By the 1970's it was understood that the two forms of invasive fire ants had been two species (the dark form, Solenopsis richteri and the red Solenopsis invicta). The differentiation between the two at the colonizing edges of the fire ant wave is a genuine hybrid zone. Shoemaker and colleagues (1996) sampled the genetics of ants in this hybrid zone, finding that genetic markers and morphological characters introgressed at different rates, and that there appeared to be selection against hybrids in contact with one or the other parental type.

Later, Ross and Shoemaker (2005) studied the genetics of these South American species (S. richteri and S. invicta) in their native ranges. They found that the species were fully reproductively isolated at study sites where both were found. Additionally, the extent of genetic differentiation between different populations of each, and the presence of a third closely related species (S. quinquecuspis) led them to suggest that the group "is actively radiating species". This would be a confirmation of Brown's (1957) argument for the high speciation potential of the central populations in the range of this genus. It remains to be seen whether these central populations have actively generated new colonizing species to displace more peripheral populations by natural movement.

In the case of fire ants, the rapid colonization of the North American invaders has been aided by some unique social changes, described by Kenneth Ross and colleagues (1996). Probably most people think of ant colonies as having a single queen and many workers and soldier ants. But some kinds of ants form colonies with multiple queens. Imported fire ants have both single-queen and multiple-queen colonies, but the size and proportion of multiple-queen colonies has greatly increased relative to their South American range. This reduces intercolony competition and facilitates their spread compared to native species.

Later work has shown that S. invicta has a genetic switch that determines whether queens will form their own colonies or whether they will remain in their natal colony or attempt to join a new one. The system is described by Tsutsui and Suarez (2003):

Queens from the two social forms typically possess different genotypes at the general protein-9 (Gp-9) allozyme locus (Ross 1997; Ross & Keller 1998; Krieger & Ross 2002 ). Monogyne colonies contain queens that are BB at Gp-9 and produce new BB queens that disperse and found colonies independently (Shoemaker & Ross 1996). Conversely, the queens in polygyne colonies are almost exclusively Bb and can produce BB, Bb, and bb queens. New Bb queens either join their natal colony or attempt to join other polygyne colonies (DeHeer et al. 1999). Any BB queens that attempt to join polygyne colonies or reproduce within them are killed by the Bb workers present in polygyne colonies (Ross & Keller 1998). Studies of queen dispersal have shown that newly produced polygyne queens with the BB genotype, who are doomed to execution if they remain in their natal colony or attempt to join other colonies, may attempt to found colonies independently, but with limited success (DeHeer et al. 1999). The bb genotype appears to be lethal in workers, and fertile bb queens are extremely rare (Ross 1997; but see DeHeer et al. 1999; Goodisman et al. 2000. Interestingly, polygyne colonies in the native range can possess reproductive queens that are either BB or Bb (Keller & Ross 1999). This difference between native and introduced populations could indicate the presence of other undiscovered genes or alleles that affect queen number or could be the result of a genetic bottleneck on variation at the loci involved in this process (Keller & Ross 1999; Krieger & Ross 2002).

This is an interesting case with several elements. A simple genetic strategy is held polymorphic because the homozygotes for the multiple-queen strategy are completely nonviable. In the new founder populations, this allele might be lost completely. Also, possible modifier loci may lose alleles that restrain the formation of supercolonies in their native range.

Still, when it comes to social changes of invasive ants, nothing compares to the case of the Argentine ant (Linepithema humile). Like fire ants, the Argentine ant invaded the American South, becoming common early in the 1900's. They have also invaded California and the Southwest as well as five of the other six continents (sparing Antarctica...). In Argentine ants, the genetic uniformity of new colonizing populations is so great that the ants form supercolonies stretching across large areas. Here's a passage from a review paper by Neil Tsutsui and Andrew Suarez (2003):

Throughout their introduced range Argentine ants are highly unicolonial ( Newell & Barber 1913; Markin 1970; Keller & Passera 1989; Way et al. 1997; Suarez et al. 1999; Tsutsui et al. 2000; Giraud et al. 2002) and can attain remarkably high densities. For example, in an early attempt to eradicate Argentine ants from a 19-acre ( 7.7-ha) orange grove in Louisiana, Horton (1918 )reported trapping an astounding 1.3 million queens in artificial nest boxes over the course of 1 year. Including workers and brood, the total volume of Argentine ants collected was over 1000 gallons (Horton 1918). Although a single "supercolony" occupies virtually the entire Californian range ( Tsutsui et al. 2000), close examination has revealed several smaller "secondary" colonies (Holway et al. 1998; Tsutsui & Case 2001). The secondary colonies are spatially restricted, aggressive toward one another and toward the large supercolony, genetically distinct from one another and the large supercolony, and may be the result of separate introductions or genetic drift (Suarez et al. 1999; Tsutsui et al. 2001).

Yuck! Looking at the 20 inches of snow lining my yard is a whole lot easier when I consider how few invasive ant species have come from Siberia.

The invading Argentine ants have an even more substantial reduction in genetic diversity than fire ants, with heterozygosity being reduced to a third of its value in the native range of the ants. Not only founder effects, but also unique patterns of social behavior and selection maintain this low diversity. There is selection against genetically different colonies, who are outcompeted by supercolonies of genetically similar lineages. Also, a phenomenon called "queen execution" tends to increase the relatedness of individuals within colonies by eliminating a proportion of reproductives.

Tsutsui and Suarez (2003) present a good argument for understanding the genetics of this transformation to highly invasive phenotypes:

Finally, there are dozens of introduced ant species about which virtually nothing is known (McGlynn 1999). Many of these species may have the potential to become invasive, and prevention may be possible only if we are aware of their dispersal capabilities (both natural and human-mediated) and the factors that could facilitate their successful establishment and spread.

Invasive fire ants have recently reached California and are busily displacing the Argentine ants there. After reading through a number of articles, the final message of many of them has been that invasive species will ultimately be controlled only by the arrival of new invasive competitors.

Yippee.

References:

Brown WL, Jr. 1957. Centrifugal speciation. Q Rev Biol 32:247-277.

Callcott A-M, Collins HL. 1996. Invasion and range expansion of imported fire ants (Hymenoptera: Formicidae) in North America from 1918-1995. The Florida Entomologist 79:240-251.

Ross KG, Vargo EL, Keller L. 1996. Social evolution in a new environment: the case of introduced fire ants. Proc Nat Acad Sci USA 93:3021-3025. Abstract

Shoemaker DD, Ross KG, Arnold ML. 1996. Genetic structure and evolution of a fire ant hybrid zone. Evolution 50:1958-1976.

Tsutsui ND, Suarez AV. 2003. The colony structure and population biology of invasive ants. Conservation Biol 17:48-58. doi:10.1046/j.1523-1739.2003.02018.x

Wilson EO. 1953. Origin of the variation in the imported fire ant. Evolution 7:262-263.