THE INBREEDING PARADOX IN INVASIVE SPECIES

Julio E. Pérez, Carmen Alfonsi, Mauro Nirchio and Jorge Barrios

Julio E. Pérez. M.A. in Zoology, University of Kansas, USA. Ph.D. in Biology, University of Southampton, UK. Professor, Instituto Oceanográfico de Venezuela, Universidad de Oriente (IOV-UDO), Venezuela. Address: Instituto Oceanográfico de Venezuela, Universidad de Oriente, Cumaná, Venezuela. e-mail: jeperezr@yahoo.com

Carmen Alfonsi. M.Sc. in Marine Sciences, IOV-UDO, Venezuela. Professor, IOV-UDO, Venezuela. e-mail: calfonsi@sucre.udo.edu.ve

Mauro Nirchio. M.Sc. in Marine Sciences, IOV-UDO, Venezuela. Professor, Escuela de Ciencias Aplicadas del Mar, UDO, Venezuela. e-mail: nirchio@cantv.net

Jorge Barrios. M.Sc. in Marine Sciences, IOV-UDO, Venezuela. Professor, IOV-UDO, Venezuela. e-mail: jbarrios@sucre.udo.edu.ve

SUMMARY

One of the most relevant topics in the biology of invasion concerns an inbreeding paradox: how do exotic species that usually invade new territories in small numbers, thus suffering the effects of inbreeding, become successful invaders. To explain this paradox, it has been argued that high migration rates and repeated introductions of exotic species take place so as to overcome low genetic diversity and inbreeding. However, several single episodes of exotic species introduction have occurred that cannot be explained by this hypothesis. An attempt is made to solve this paradox by considering that invaders are not only able to modify the new environment, but also suffer modifications under the influence of the new environment. The possible role of epigenetic adaptations and adaptive mutations is postulated in order to explain the successful adaptation of invaders in their new environment.

Uno de los tópicos más relevantes en la biología de las invasiones se refiere a la paradoja de la consanguinidad: cómo especies exóticas, que generalmente invaden nuevos territorios en pequeños números, sufriendo por lo tanto los efectos de la consanguinidad, se convierten en invasores exitosos. Para explicar esta paradoja, se ha argumentado que en ocasiones han ocurrido altas frecuencias de migración e introducciones repetidas, que han superado la baja diversidad genética y la consanguinidad. Sin embargo, varios casos de introducciones simples de especies exóticas han ocurrido que no pueden ser explicados por esta hipótesis. Para intentar resolver esta paradoja consideramos que los invasores no solamente son capaces de modificar sus nuevos ambientes, sino que también sufren modificaciones bajo la influencia de estos ambientes. Se postula el posible papel de las adaptaciones epigenéticas y de las mutaciones adaptativas para explicar la adaptación exitosa de los invasores a sus nuevos ambientes.

Resumo

Um dos tópicos mais relevantes na biologia das invasões se refere ao paradoxo da consangüinidade: como espécies exóticas, que geralmente invadem novos territórios em pequenos números, sofrendo por tanto os efeitos da consangüinidade, se convertem em invasores exitosos. Para explicar este paradoxo, tem-se argumentado que em ocasiões tem ocorrido altas freqüências de migração e introduções repetidas, que têm superado a baixa diversidade genética e a consangüinidade. No entanto, varios casos de introduções simples de espécies exóticas têm ocorrido que não podem ser explicados por esta hipótese. Para tentar resolver este paradoxo consideramos que os invasores não somente são capazes de modificar seus novos ambientes, senão que também sofrem modificações sob a influência de estes ambientes. Postula-se o possível papel das adaptações epigenéticas e das mutações adaptativas para explicar a adaptação exitosa dos invasores a seus novos ambientes.

The loss of genetic variation due to genetic drift and the effects of inbreeding are though to be major factors in the extinction rate of small populations. For example, it is widely assumed that inbreeding and loss of genetic diversity reduce disease resistance (Spielman et al., 2004; Frankham, 2005a). These authors tested whether inbreeding and loss of genetic diversity do affect a host´s resistence to disease; Drosophila melanogaster populations with different levels of inbreeding were separately exposed to thuringiensin, an insecticide toxin produced by some strains of Bacillus thuringiensis, and to live Serratia marcescens bacteria. Inbreeding and loss of genetic diversity reduced resistance of D. melanogaster to both thuringiensin toxin and live S. marcescens.

The introduction of alien species involves a population bottleneck because the number of initial colonists is small, a harmful situation resulting from inbreeding and genetic drift, factors that would contribute to the extinction of the invaders. Thus, a newly established population is likely to be genetically much less diverse, than the population from which it is derived. The loss of genetic variation through genetic drift and the inbreeding effect on small populations are thought to increase their extinction rate (Saccheri et al., 1998; Allendorf and Lundquist, 2003).

Frankham (2005b) recently indicates that propagule pressure, which includes the number of individuals introduced and the number of release events, sometimes from different sources, will produce invasive species that are not as genetically poor as expected, partially explaining the successful invasion of some species. Also, Lockwood et al. (2005) indicated that of all the different factors that determine a favorable introduction outcome, propagule pressure was emerging as a single consistent correlate of establishment success. Occasionally, and due to hybridization between individuals from genetically divergent native populations, introduced populations will have more genetic variation than native populations of the same species (Dupont et al., 2003; Kolbe et al., 2004). Hybridization is recognized as an important factor in the success process after introduction of alien species (Facon et al., 2005). Although this explanation seems to resolve the paradox, it is not useful to explain several successful invasions where only a single inoculation occurred. Three examples are:

1- Tilapia, Oreochromis mossambicus, was introduced into Venezuela's Laguna de los Patos (10º25'42''N, 64º11'36''W), a small fresh water lake with marine water influence, in 1964. Tilapia was directly or indirectly responsible for the disappearance of 13 out of 23 native species of fish (Aguilera and Carvajal, 1976). The introduced O. mossambicus juveniles, were descendants of 17 adult specimens imported from Trinidad (Holt, 1965), and produced in the Fish Culture Station of El Limón, in Venezuela. Inasmuch as O. mossambicus was first exported from Africa to Asia, and later throughout the world (Costa-Pierce, 2004), it is most likely that the species arrived at Trinidad from Asia. Therefore, the specimens introduced in Laguna de los Patos suffered at least four bottlenecks. This species is currently present in most of the Manzanares River, near Laguna de los Patos, where it has contributed to the elimination of 6 native fish species (Pérez et al., 2003), as well as in coastal marine waters.

2- The marine alga Kappaphicus alvarezii, was successfully introduced in two restricted areas of the eastern coast of Venezuela in 1996 from cultures in the Philippines, where it has remained infertile during at least 25 years of intensive rope cultivation (Rincones and Rubio, 1999). Its distribution (Barrios, 2005) is now rapidly spreading vegetatively in the absence of sexual reproduction, through tallus fragmentation.

3- The amphibian Rana catesbiana, or American bullfrog, was introduced without authorization in the town of Jají, in the Venezuelan Andes (Ojasti et al., 2001) in the 90s. Its general eating habits, high mobility and, above all, its highly reproductive capabilities, have made bullfrogs extremely dangerous and threatening to biodiversity. The introduction consisted of two couples, at the most, but the invasion is now hard to stop, although personnel from the Venezuelan Ministry of the Environment and Natural Resources is doing everything possible to eradicate this plague (Edis Solórzano, personal communication).

This kind of single successful introductions point a need to look for additional hypotheses to solve the ensuing paradox.

The reductionistic view that organisms can be understood by the properties of their genes and nothing else must be critically assessed, because it is an impediment to understanding invasions. Genes make sense only within the context of whole organisms, and more goes into the making of the whole organism than just its genes (Kardong, 2003). In population biology there is a tendency to analyze adaptation and selection in terms of one or at most a few loci.

The final impediment to resolving the paradox is the so called central dogma of molecular biology. The theory states that the DNA sequence is transcribed into RNA, and that the RNA is translated into specific sequence of amino acids. The information flows in a one-way direction; there is no reverse flow of information. As might be expected, this suggests that environmental influences do not affect genes. Organisms are a purely deterministic product of some collection of genes. Although people accept that the environment interacts with organisms to change some of their characteristics, it is generally accepted that the germline is stable and does not change under the influence of the environment. However, evidence that genes are not immune to environmental influences has been accumulating in the findings of molecular genetics.

a) Meneses and Santelices (1999) postulated that genetic variation in Gracilaria chilensis, which mainly reproduces asexually by fragmentation, can arise via somatic mutations and mitotic recombination that can occur through ramet replication, and that the effect of genetic motile elements (ie. transposons) would increase the genetic variation within a clone.

b) Recent developments in the weedy cress Arabidopsis thaliana indicate a mechanism that can improve genetic variation through mutant genes repaired by using RNA templates inherited from earlier generations but not present in their parents (Lolle et al., 2005). This mechanism would allow plants to "experiment" with new mutations. If the mutation proves to be harmful it will, with the help of the RNA, revert to their grandparents’ DNA sequence in the next generation.

c) The possibility that epigenetic changes in gene functions would allow invaders to become established in the short term must be considered. Waddington (1953) coined this term to refer to processes by which inheritable modifications in gene function occur but are not due to changes in the base sequence of the organism’s DNA; the sequence remains unaltered. Only the environment of mechanical, nutritional, chemical, and biotic factors such as predator presence is modified and affects the phenotypic expression.

d) The discovery of "adaptive" mutation in bacteria shook the dogma that gene mutation occurs at random and independent of the environment in which the organism lives by suggesting the existence of a new kind of mutation, one that differed from spontaneous mutation. "Adaptive mutation" refers to a collection of processes in which cells respond to growth-limiting environments by producing compensatory mutants that grow well, apparently violating fundamental principles of evolution (Hastings et al., 2004; Ho, 2004). In general, this kind of mutation appears to be induced by stress (Rosenberg and Hastings, 2004). To accept even the possibility that not all mutations occur at random has been so heretical that most biologists simply dismiss the idea without critically evaluating the evidence which shows that, in some cases, adaptive mutation almost certainly occurs (Rosenberg, 2001; Bjedov et al., 2003; Elena and Lenski, 2003; Rosenberg and Hastings, 2003, 2004; Hastings et al., 2004). In eukaryotes, Denver et al. (2004) have suggested that cellular stress response might provoke hypermutation in the roundworm Caenorhabditis elegans. Most of these mutations would surely prove harmful or be neutral, but rare adaptive mutations would also occur, allowing some rare individuals in stressed populations to flourish (Rosenberg and Hastings, 2004).

Undoubtedly, an invasion is a stress condition and lends support to the idea that evolution might be hastened under stress. Furthermore, epigenetic changes could help in the immediate adaptation of invasive species (Pérez et al., 2006). Invaders could be epigenetically "preadapted" to the new environment. Balter (2000) suggested that epigenetic changes could play an adaptive role.

If the differences are greater, there will be no invasion or a time lag would be present, until adaptive mutations arise and become established in the future invaders, keeping in mind that low numbers of organisms would contribute to the fixation.

Another explanation to the successful introduction of some species is given by the biotic regulation concept (Gorshkov et al., 2004). According to this concept, species of the natural ecological community have collectively evolved some restrictions on their functioning that serve to stabilize the community as a whole. Invasive species do not carry genetic information about ecological restrictions (Makarieva et al., 2004). Exotic organisms can be a source of perturbation acting in an uncorrelated manner with other organisms so as to prevent the community from efficiently controlling environmental conditions. If this effect is strong enough, the local environment of such a community will begin to deteriorate. As soon as the degree of deterioration becomes significant, all inhabitants of the local ecological community will lose competitivity, and alien species will encounter at least the same conditions as the other species.

Although there is the possibility that the paradox does not exist, in the sense that reduction in genetic variation will not pose a challenge for the invading species, we believe that, as seen from a few experimental field studies, there is ample evidence of fitness reduction due to inbreeding in captivity. Also, in the Glanville fritillary butterfly, Melitaea cinxia, Saccheri et al. (1998) found the first demonstration of the effect of inbreeding on the extinction of natural populations, an extinction risk significantly increased with decreasing heterozygosity.

More research is required to establish the genetic basis of traits related to the establishment and spread of invasive species. These traits cannot be analyzed with protein and DNA markers, although mapping quantitative traits affecting fitness (QTLs) may be possible (Sakai et al., 2001; McKay and Latta, 2002). Quantitative trait loci (QTL) mapping analysis methods and associated computer programs provide tools that allow evolutionary studies on the genetic bases of multiple trait variation (Zeng, 2005). These recent developments have great importance for the study of the biology of invasions.

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