Bioinvaders: The acquisition of new genetic variation.

Julio E. Pérez, Carmen Alfonsi, Mauro Nirchio and Sinatra K. Salazar

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

Carmen Alfonsi. Dr. in Zoology. Universidad Central de Venezuela. Professor, IOV-UDO, Venezuela.

Mauro Nirchio. M.Sc. in Marine Sciences, UDO, Venezuela. Professor, Escuela de Ciencias Aplicadas del Mar (ECAM-UDO), Venezuela.

Sinatra K. Salazar. MSc. in Marine Sciences. UDO, Venezuela. Professor, ECAM-UDO, Venezuela.

SUMMARY

Given that the introduction of organisms into a new environment usually occurs in low numbers, reducing genetic diversity (the so-called bottleneck effect), and that selection further decreases diversity beyond that caused by the bottleneck, then how do some alien species, if their genetic variation is low under new conditions, succeed in evolving rapidly, becoming invasive and expanding their ranges? In this paper a series of mechanisms that allow the introduced population to acquire new genetic variations are considered. Various possible roles of epigenetic adaptation, hybridization, adaptive mutations, transposons, endosymbiosis, somatic mutations, and mitotic recombination are postulated as sources of new genetic variations. The roles of purging and biotic regulation in the successful invasions of some species is also analyzed.

Bioinvasores: Adquisición de nueva variación genética.

RESUMEN

La introducción de organismos a un nuevo ambiente generalmente ocurre en escaso número de individuos, lo cual determina el llamado "cuello de botella", reduciendo la variación genética, mientras que la selección reduce aún más esta variación. Entonces, ¿Cómo estos exóticos son exitosos, expanden su rango de distribución bajo nuevas condiciones, evolucionan rápidamente y se convierten en invasores, si su variación genética es baja? En el presente trabajo, se consideran una serie de mecanismos que permitirían a las poblaciones introducidas adquirir nueva variación genética. Las adaptaciones epigenéticas, la hibridización, las mutaciones adaptativas, los transposones, la endosimbiosis, las mutaciones somáticas y recombinaciones mitóticas son postuladas como fuentes de nueva variación. Además se analiza el papel de la purificación y la regulación biótica en la invasión exitosa de algunas especies.

Bioinvasores: Aquisição de nova variação genética.

RESUMO

A introdução de organismos a um novo ambiente geralmente ocorre em escasso número de indivíduos, o qual determina o chamado "efeito gargalo", reduzindo a variação genética, enquanto que a seleção reduz ainda mais esta variação. Como, então, podem estes exóticos ser bem sucedidos, expandir sua faixa de distribuição sob novas condições, evolucionar rapidamente e se converter em invasores, se sua variação genética é baixa? No presente trabalho, é considerada uma série de mecanismos que permitiriam às populações introduzidas adquirirem nova variação genética. As adaptações epigenéticas, a hibridização, as mutações adaptativas, os transposões, a endossimbiose, as mutações somáticas e recombinações mitóticas são postuladas como fontes de nova variação. Além disso, se analisa o papel da purificação e a regulação biótica na invasão bem sucedida de algumas espécies.

KEYWORDS / Biotic Regulation / Endosymbiosis / Epigenetics / Purge /

Received: 02/18/2008.  Modified: 10/15/2008.  Accepted: 10/23/2008. 

Introduction

It is commonly assumed that preserving genetic diversity is absolutely necessary for species to continue to adapt genetically in a changing environment. The introduction of alien species, however, produces a population bottleneck because the number of initial colonists is small, and a harmful situation is likely to occur due to inbreeding and genetic drift, factors that would contribute to the extinction of the invaders. During the introduction of aliens, bottlenecks reduce diversity in neutral genes, and selection decreases diversity beyond that caused by the bottleneck. Loss of genetic variation is determined by the effective minimum (or founder) population size (Ne) and the growth rate of the population. As indicated by Dlugosch and Parker (2008), lower Ne and/or null growth rate lead to the loss of alleles, particularly those that are rare. Furthermore, several exotic species are apparently not genetically adapted to their new environment (Pérez et al., 2006a, b).

In the biology of invasions it is usually assumed that loss of genetic variation due to the low numbers of exotic organisms introduced reduces the capacity, called adaptive potential or evolvability (Houle, 1992), of small populations to evolve in response to new environmental conditions (Reed and Frankham 2003; Pérez et al., 2006a, b).

Then, how are some alien species so successful in expanding their ranges under new conditions, evolving rapidly, and becoming invasive, if their genetic variation is low? Is it because genetic variation is not necessary? Spielman et al. (2004) answered this question, comparing average heterozygosity in 170 threatened taxa with that in taxonomically related non-threatened species. Heterozygosity was lower in threatened taxa in 77% of comparisons, a highly significant departure from the predictions of the hypothesis of no genetic impact.

Genetic variation has been examined using molecular markers to measure the amount of genetic diversity in invasive populations. Molecular genetic markers appear to be poor indicators of heritable variation in adaptative traits (McKay and Latta, 2002). Recent analyses (Bensch et al., 2006) have questioned the usefulness of heterozygosity estimates as measures of the inbreeding coefficient (f) and confirm that f and heterozygosity are poorly correlated in a wild and highly inbred Scandinavian wolf population (Canis lupus). Nevertheless, they recommend that management programs of endangered populations include estimates of both f and heterozygosity, as they may contribute complementary information about population viability.

More research is required to establish the genetic basis of traits related to the establishment and spread of invasive species, traits that are probably under polygenic control and significantly influenced by the environment. These traits cannot be analyzed with protein and DNA markers, although mapping of quantitative traits loci (QTL) affecting fitness may be possible (Sakai et al., 2001, McKay and Latta, 2002). QTL mapping analysis methods and associated computer programs provide tools that allow evolutionary studies on the genetic basis of multiple trait variation (Zeng, 2005).

On occasion, the diminution of genetic variation seems to have contributed to successful invasions, as occurred in the invasion of North America by the Argentine ant (Linepithema humile). Studies using microsatellite markers have shown that the Argentine ant populations introduced in California possess only about 50% of the alleles and 1/3 the expected heterozygosity of native populations. The introduced population is genetically homogeneous over large distances (up to 1000km), whereas native populations maintain their genetic structure over tens to hundreds of meters (Tsutsui et al., 2000; Tsutsui and Case, 2001). In their indigenous range, L. humile populations consist of colonies that contain multiple nesting sites, each colony territory being aggressively defended against other Argentine ant colonies. In contrast, virtually all Argentine ants in California belong to the same supercolony. The success of this invasion has been interpreted as resulting from the diminution in intraspecies aggression and subsequent supercolony formation, probably due to a reduction of recognition alleles that prevent individuals from discriminating nestmates from non-nestmates based on genetic similarity (Tsutsui et al., 2000, 2003; Tsutsui and Case, 2001).

Furthermore, the inappropriate application of some approaches to invasion processes, such as reductionism and the central dogma of biology (information flows in only one direction: DNA is transcribed into RNA, and RNA is translated into protein; no reverse flow of information takes place) has delayed the understanding of the invasive process. In reductionism, it is emphasized that genes make sense only within the context of whole organisms, and that more goes into the making of the whole organism than just its genes. Singh (2003) commented that classical experimental population genetics dealing with genetic polymorphism and estimation of selection coefficients on a gene-by-gene basis is coming to an end, and a new era of interdisciplinary and interactive biology focusing on dynamic relationships among genes, organisms, and environment has begun. On the other hand, evidence that genes do not remain unaffected by environmental influences has been accumulating in the findings of molecular genetics. Epigenetic inheritance is just one possible mode of reverse information flow from the environment to the genome (Kardong, 2003).

Ways to Increase Genetic Variation

Although an increase or decrease in fitness in a population depends mainly on the size and the distribution of mutational effects, there are several other mechanisms that would allow the introduced organisms not only to increase their genetic variation, but also to adapt to new environments (Figure 1).

Propagule pressure and hybridization

Hybridization is recognized as an important success factor subsequent to the introduction of alien species (Facon et al., 2005; Rieseberg et al., 2003). Due to hybridization between individuals from different propagules, introduced populations will occasionally have a larger genetic variation than native populations of the same species (Dupont et al., 2003, Kolbe et al., 2004).

Hybridization is a genomic creativity mechanism known to make species more likely to be successful in invading novel ecosystems. Supporting evidence is found in sunflowers (Reiseberg et al., 2003) for the viewpoint that hybridization is a powerful evolutionary force that creates opportunities for adaptive evolution and facilitates ecological divergence. Species found in the most extreme habitats are ancient hybrids. Most trait differences in ancient hybrids could be recreated by complementary gene action in synthetic hybrids and were favored by selection. Hybridization provides genetic variation in hundreds or thousands of genes in a single generation, given a mechanism for large and rapid adaptive transitions such as the colonization of discrete and divergent ecological niches (Reiseberg et al., 2003).

Frankham (2005) indicated that propagule pressure (that includes the number of individuals introduced and the number of release events, sometimes from different sources) will produce invasive species less genetically poor than expected, and partially explain the successful invasion of some species. Several authors (Lockwood et al., 2005; Kelly et al., 2006; Dlugosch and Parker, 2008; Ficetola et al., 2008; Marrs et al. 2008) indicated that among factors that determine introduction success, propagule pressure is emerging as a single consistent correlate of establishment success.

On the other hand, although hybridization increases genetic variation and successful invasions, in many cases it does not explain several successful invasions in which only a single inoculation occurred. Three examples cited by Pérez et al., (2006a, b) in Venezuela are: the tilapia, Oreochromis mossambicus, introduced in 1959, after three or four bottlenecks; the marine alga Kappaphicus alvarezii, introduced in 1996 (Rincones and Rubio, 1999) expanded its range to most of the northeastern coast of Venezuela (Barrios, 2005); and the bullfrog, Rana catesbiana, introduced as one or two couples in the Venezuelan Andes (Ojasti et al., 2001).

Epigenetic changes and phenotypic plasticity

The possibility that epigenetic changes in gene functions would allow invaders to become established must be considered in the short term. It is very important to keep in mind that possible adaptative changes due to epigenetic changes could, in some cases, also be interpreted as evidence for phenotypic plasticity induced by variation in the environment.

Waddington (1953) coined the term "epigenetics" to refer to processes by which heritable modifications in gene function occur, but are not due to changes in the base sequence of the DNA of the organism. The sequence remains unaltered; only the environment of mechanical, nutritional, chemical, and biotic factors such as the presence of predators is modified and affects the phenotypic expression. The term could also be defined as the analysis of the normal non-genetic processes that influence the characteristics of the phenotype during the lifetime of the organism, historical influences included (Kardong, 2003).

Esteller (2005) suggested that it is possible to lump within the scope of the enigmatic term "epigenetics" all the heritable changes in gene expression patterns that are based on factors other than straightforward DNA sequences. The mechanisms controlling epigenetics are very complex.

On the other hand, phenotypic plasticity is the ability of a single genotype to alter its phenotype in response to environmental conditions (Nussey et al., 2005). Theoretical and laboratory research suggest that phenotype plasticity can evolve under selection. Nussey et al. (2005) demonstrated for the first time that this is also true in the wild, and presented evidence from a Dutch population of great tits (Parus major) for variation in individual plasticity in the timing of reproduction. They also showed that this variation is heritable. They have shown that this plasticity is truly advantageous and should thus become more common with natural selection.

Hereunder, two examples of adaptation are given, one due (according to the authors) to epigenetic change and the other to phenotypic plasticity:

If two species of rotifers (Brachionus calyciflorus and Karatella tropica) are placed in an environment with their natural predator, another rotifer of the genus Asplanchna, they will grow protective spine-like projections. In this case, biotic information from the environment (epigenomic influence) initiates gene action. In rotifers, spine production might be energetically expensive, or interfere with some other aspect of life, so preprogramming spines genetically and expressing them before a predator threatens may be disadvantageous (Kardong, 2003). When predators threaten rotifers, epigenomic cues activate genes that in turn produce protective spines; these epigenomic influences (predator) have already been assimilated into the genome of each, a consequence of fast evolution. Thus assimilated and preprogrammed into the genome, these epigenomic influences help explain the character of the phenotype, but are not themselves an independent cause of the phenotype (Kardong, 2003).

An example of phenotypic plasticity has been illustrated by Meimberg et al. (2006) explaining the introduction and successful invasion of the barbed goatgrass, Aegilops triuncialis, from both the Mediterranean Basin and Asia into California, despite their genomic uniformity. Although the authors initially suspected that the recent invasive spread of this grass would have resulted from the recombination of genotype from multiple introductions, results suggested that this had not occurred. Molecular data indicate that the two introductions are composed of highly uniform populations. The capacity of A. triuncialis to expand its range in California despite this strong genetic bottleneck suggests that phenotypic plasticity may be important for adaptation in this species.

In conclusion, although in epigenomic changes there is a gene alteration that allows a response to environmental changes, and in phenotypic plasticity the answer seems to be based on the amplitude of the gene action, both processes increase the chance that an introduced organism could become an invasor, and the processes are difficult to separate.

Dynamics of mutational effects, adaptive mutation,and hypermutation

Very few mutations improve the adaptation ability of an organism, and the great majority are harmful. In a recent study Silander et al. (2007) argue that the mutational effects are dynamic and not fixed, and that the same mutation occurring in a poorly adapted individual is more likely to be beneficial than if it occurs in a well adapted one. According to Betancourt (2007), the study of Silander et al. (2007) suggests that very small populations (as occurring in bioinvasions), which tend to accumulate harmful mutations, will be protected from the endless accumulation of more harmful mutations by an increasing rate of beneficial ones. In their work, Silander et al. (2007) found that some low-fitness viruses were able to maintain or even improve their fitness. Sanjuan and Elena, 2006) suggested that mutations might behave differently in viruses than in more complex organisms. The results of Silander et al. (2007) are consistent with what has been found in some studies with more complex organisms (Betancourt 2007).

The basis of genetics and the Neo-Darwinian Theory of evolution suggest that gene mutation occurs at random and is independent of the environment in which the organism lives. The discovery of ‘adaptive’ mutation in bacteria shook the dogma 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). In general, this kind of mutation appears to be induced by stress (Rosenberg and Hastings, 2004) and may speed evolution and invasions. Both the mutation mechanisms and their control by stress have remained elusive. However, Ponder et al. (2005) provide evidence that the molecular basis for stress-induced mutagenesis in an Escherichia coli model is error-prone DNA double-strand break repair.

Denver et al. (2004) have suggested that a cellular stress response in eukaryotes might provoke hypermutation in Caenorhabditis elegans. Most of these mutations would surely prove to be harmful or neutral, but in isolated cases adaptive mutations would occur, allowing some rare individuals in stressed populations to flourish (Rosenberg and Hastings, 2004). Undoubtedly, invasion is a stress condition, and lends support to the idea that evolution might be hastened under stress.

Endosymbiosis

Endosymbiosis basically involves the fusion of the entire genomes of two organisms and overlaps with horizontal gene transfer. Syvanen (1994) considered these to be one part of the larger phenomenon of cross-species gene transfer, which involves, in addition to endosymbiotic fusion, the insertion of smaller genetic regions, including single genes or even parts of genes. The mechanisms of transfer will likely involve a virus, direct transformation, conjugation, or another as yet to be investigated means.

Endosymbiosis is an evolutionary change arising from the interaction of different species at the level of the genomes. As suggested by Ryan (2006), endosymbiotic viruses might offer novel genetic and genomic complexity that would make invasion of new environments more successful. The most familiar example of viral-eukaryotic symbiosis occurs in the parasitoid wasp-polydnaviruses interactions, in which the virus carries the essential genes required to suppress the immune system of the lepidopteran host of the wasp (Wren et al., 2006). In many such examples, the viral genome has been integrated into the wasp genome. It is becoming clear that endosymbiotic unions of viruses and hosts are far from unusual and have influenced the evolution of life throughout most, if not all biodiversity (Ryan, 2006). Roossink (Frank P. Ryan, personal communication) examined symbiotic viruses that made grasses more resistant to drought conditions.

Once viruses enter a genome, their capacity for evolutionary innovation remains persistently active and can interact with newly arrived exogenous viruses or with other genetic components and regulatory mechanisms, thus increasing evolutionary plasticity (Lower et al., 1996, cited by Frank P. Ryan 2006).

Hotopp et al. (2007) found what seems to be the entire genome of a parasitic bacterium, Wolbachia pipientis, inserted in the genome of the fruit fly, Drosophila ananassae. The discovery suggests that the bacterial genome must have provided some sort of evolutionary advantage to its host. This species is a maternally inherited endosymbiont that infects a wide range of arthropods, including at least 20% of insect species, as well as filarial nematodes. It is present in developing gametes and passes from one female to another through infected ova, providing circumstances conducive to heritable transfer of bacterial genes to the eukaryotic hosts.

Chisholm et al. (1996) showed that the rhizoids of the giant alga Caulerpa taxifolia function as roots. Examination of the rhizoids revealed that the outer surface is coated with a mixture of bacteria; the cytoplasm contains large numbers of rod-shaped bacteria with the ability to take up inorganic phosphorous and organic nitrogen from substrata and translocate nutrient products to the photoassimilatory organs. The endosymbiosis explains the alga´s ability to proliferate in oligotrophic waters.

Transposons

Small packages of DNA can splice into other sequences and provide fortuitous opportunities for evolutionary innovations. Transposons seem to appear suddenly in a genome, copying, cutting and pasting themselves throughout its chromosomes (Pennisi, 2007). Transposable elements might be responsible for some genomic rearrangements that could provide an important substrate for adaptation during invasion (Lee, 2002).

Kalendar et al. (2000) found in specimens of the wild ancestor of cultivated barley (Hordeum spontaneum) collected in Evolution Canyon, Mount Carmel, Israel, from various microclimates, that a particular type of retrotransposon, called BARE-1, is up to three times more abundant in barley plants growing at the canyon rim than those growing near the bottom of the canyon. This suggests that plants at higher elevations gain more and lose fewer copies than plants farther down. The authors speculate that a larger genome, achieved through the ample presence of retrotransposons, may help plants deal with the more stressful high and dry areas of the canyon, by influencing the physiological machinery that enables the plant to seek or retain water.

Retrotransposons are a principal component of most eukaryotic genomes, representing ~40% of the human genome and 50-80% of some grass genomes. They are usually transcriptionally silent but can be activated under certain situations of stress. Despite their considerable contribution to genome structure, their impact on the expression of adjacent genes is not well understood (Kashkush et al., 2002).

Somatic mutations and mitotic recombination

In the species that mainly reproduce asexually by fragmentation, such as the alga K. alvarezii K. alvarezii, genetic variation can arise through somatic mutations and mitotic recombination that can occur through branch (ramet) replication and would increase the genetic variation within a clone. Chapman et al. (2000) reveal variable levels of genetic variation in the clonal weedy species Pilosella officinarum (Asteraceae) of New Zealand, introduced from Europe in the late 19^th century. Somatic recombination and somatic mutations contribute to increased genetic variation and partially explain why this species is such a successful invader in New Zealand.

RNA

Small regulatory RNAs (microRNAs; siRNAs and piRNA) can exert regulation at the transcriptional level, by affecting chromatin structure (epigenetic regulation), or post-transcriptionally, by affecting mRNA stability or translation. Animals and plants have hundreds of distinct microRNA genes whose developmental regulatory roles are most clearly evident in the small RNAs, as confirmed by genetic studies in model organisms (Ambros and Chen, 2007).

Phylogenetic studies suggest that microRNA-based gene regulation emerged early during the evolution of both plants and animals, and indicate that it played a role in adaptative diversification. Many microRNAs and their target interactions appear to be rapidly evolving, suggesting an ongoing potential for microRNAs to drive animal and plant diversity. Now, one of the many immediate challenges is to elucidate how small RNAs mediate the epigenetic regulation of gene expression (Ambros and Chen, 2007).

Other Mechanisms

Among several other mechanisms that increase the chances of introduced species becoming invasive, biotic regulation and purge (Figure 1) are next examined in detail.

Biotic regulation

Another explanation for the successful introduction of some species is given by the biotic regulation concept (Gorshkov et al. (2004); www.biotic-regulation.pl.ru/bre-vers.htm). According to this concept, species of the natural ecological community have collectively evolved 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 the other organisms, 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 competitiveness and alien species will encounter at least the same conditions as the other species.

Purge

Often the offspring produced by the mating of close relatives are less fit than that produced by mating of unrelated individuals (i.e., inbreeding depression, ID). This is a common situation in bioinvasion, due to the low number of introduced exotics. This loss of fitness has been explained by the increased probability of expressing deleterious recessive alleles in the inbred offspring (the "partial dominance" model). If most inbreeding depression is due to deleterious recessive alleles, it is possible that the severity of inbreeding depression can be diminished if natural selection can purge such alleles from the population during inbreeding (Swindell and Bouzat, 2006). The influence of inbreeding on fitness-related traits in endangered species and other organisms appears to be variable over populations, traits, and environment. Leeberg and Firmin (2008) indicate that although purging is an important process in many small populations, the literature contains a diversity of responses.

An interesting case of inbreeding, apparently without consequences in fertility, occurs in the Chillingham cattle that live in isolation in a park in northern England. Although they have been inbred for at least 300 years, the herd remains as fertile as ever (Visscher et al., 2001), despite a population crash in 1947 that left only eight bulls and five cows. DNA analyses show that the 49-strong herd is almost a clonal organism, a fact unprecedented in mammals. Visscher et al. (2001) indicate that their findings support the theory that while inbreeding is on average bad for a population, it can occasionally result in a viable population. When combined with selection, inbreeding may purge deleterious alleles. This successful purging probably happens infrequently, as previous research suggests that inbreeding usually does weaken a population.

At present the herd is feral, but there may have been some human help in the gene purging during domestication. Hall, cited by E. Young (2001), indicated that during domestication genes that tolerate inbreeding are selected. If genes that promote tolerance of inbreeding do exist, tracking them down may be important for the successful breeding of small numbers of endangered species in the future.

Acknowledgements

The authors thank Frank P. Ryan, Sheffield South West Primary Care Trust, Sheffield, UK, for calling our attention to the role of endosymbiosis in bioinvasions.

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