Range expansion by invasive species

Red flour beetle (Tribolium castaneum (Herbst)) has been a model species for study of influences of demography (birth, death and dispersal) and genetics on range expansion by invasive species. Demography and genetics had important and independent roles in colonization success in nutritionally challenging environment. Inbreeding had negative effects while outbreeding had positive effects on population growth and long-term establishment. Prior adaptation to the environment rivaled the importance of number and size of introductions. Adults emigrated more and further from a high-density than a low-density population. These studies are important to predicting likelihood of establishment, preventing establishment of new pest species and successfully introducing new natural enemies. On a local level, T. castaneum is an invasive species each time it colonizes an uninfested commodity or facility.

Establishment increased with number of founders (43% with 2 to 100% with 32), inbreeding and environment quality reduced population growth, and genetic diversity and environment quality increased dispersal (Szűcs et al. 2014). Establishment increased more over 7 generations with several, smaller introductions than with one or two large introductions (Koontz 2014, Koontz et al. 2018). Establishment was not affected by biologically realistic fluctuations in nutritional quality of food with up to 99% corn flour. Focken (2007) showed that red flour beetles develop faster and reproduce more on wheat flour than corn flour and suggested that larvae may be able to distinguish between particles of corn and wheat in mixtures. Both demography and genetics had important and independent roles in colonization success in nutritionally challenging environment (96.3% corn flour, 3.515 % wheat flour, and 0.185 % brewer’s yeast) over 7 generations in an array of linearly interconnected food patches allowing dispersal between patches (Szűcs et al. 2017a). Inbreeding had negative effects while outbreeding generally had positive effects on establishment, population growth and long-term persistence. Extinction risks depend upon environmental stochasticity, demographic stochasticity, and demographic heterogeneity (Melbourne and Hastings 2008) and variation in spread rates among replicates was high (Melbourne and Hastings 2009). Genetic diversity can overcome predicted high extinction risk in new habitats (Agashe et al. 2011). Spatial evolution has a significant 6% higher mean spread rate and heightened variability in spread rates compared with the shuffled treatment in which spatial evolution was prevented (Weiss-Lehman et al. 2017). Higher dispersal ability and lower intrinsic growth rates evolve at the expansion edge.

Prior adaptation to the environment rivaled the importance of number of introductions and the number of individuals per introduction in determining the establishment success and size of founding populations (Vahsen 2017, Vahsen et al. 2018). Within six generations, evolving populations expanding range into a nutritionally challenging environment grew three times larger and spread 46% faster than populations in which evolution was constrained (Szűcs et al 2017b). Over the course of six generations, genetic rescue by replacing individuals from laboratory cultures with field strain increased population sizes and intrinsic fitness (Hufbauer et al. 2015). Genetic rescue is constrained by genetic load (Stewart et al 2017). Demographic and genetic rescue reduced extinction, and those effects were additive. Individuals, on average, were 21.4% more likely to emigrate (i.e. disperse from the first patch) when dispersing from a high-density than a low-density environment (Endriss et al. 2019). Individuals were also more likely to disperse further. Prior juvenile density strongly mediated the effect of current density on dispersal. Interspecific competition dramatically slows expansion across a landscape over multiple generations (Legault 2017, Legault et al. 2020). Nutritional quality of natal wheat flour and new oat flour habitat also influenced population growth (VanAllen and Rudolf 2013) and emigration (VanAllen and Bhavar 2014). Nutritional quality of natal habitat also can alter outcome of competition in new oat flour habitat (VanAllen and Rudolf 2015, 2016).  

Initial studies found that egg or pupal cannibalism by larvae and adults in populations closed to dispersal determined outcome of competition between Tribolium species (Sokoloff 1974). Alabi et al. 2008 determined variation in cannibalism by developmental stage and species. More recently allelopathic chemicals conditioning of flour has been shown to influence life history and may be important in intra- (Khan et al. 2018) and interspecies (Bullock et al. 2020) competition. Fecundity of T. confusum was largely unaffected by flour conditioned by T. castaneum, T. castaneum fecundity was reduced by flour conditioned by either species and conditioning by the other species decreased development times for each species.

References

Agashe D, Falk JJ, Bolnick DI 2011. Effects of founding genetic variation on adaptation to a novel resource. Evolution 65(9):2481-91.

Alabi T, Michaud JP, Arnaud L, Haubruge E. 2008. A comparative study of cannibalism and predation in seven species of flour beetle. Ecol. Entomol. 33:716-26.

Bullock, Marissa, Geoffrey Legault, and Brett A. Melbourne. 2020. Interspecific chemical competition between Tribolium castaneum and Tribolium confusum (Coleoptera: Tenebrionidae) reduces fecundity and hastens development time. Annals of the Entomological Society of America 113(3): 216-222.

Endriss SB, Vahsen ML, Bitume EV, Monroe JG, Turner KG, Norton AP, Hufbauer RA. 2019. The importance of growing up: juvenile environment influences dispersal of individuals and their neighbours. Ecol. Let. 22:45-55.

Focken U. 2007. Effect of different ratios of wheat to corn flour in the diet on the development and isotopic composition (δ13C, δ15N) of the red flour beetle Tribolium castaneum. Isotopes in environmental and health studies 43:143-154.

Hufbauer RA, Szűcs M, Kasyon E, Youngberg C, Koontz MJ, Richards C, Tuff T, Melbourne BA. 2015. Three types of rescue can avert extinction in a changing environment. PNAS 112: 10557-10562.

Khan I, Prakash A, Issar S, Umarani M, Sasidharan R, Masagalli JN, Lama P, Venkatesan R, Agashe D. 2018. Female density-dependent chemical warfare underlies fitness effects of group sex ratio in flour beetles. Am. Nat. 191: 306–317.

Koontz, Michael. 2014. Eco-evolutionary consequences of multiple introductions for colonizing individuals. MS thesis, Colorado State University.

Koontz MJ, Oldfather MF, Melbourne BA, Hufbauer RA. 2018. Parsing propagule pressure: Number, not size, of introductions drives colonization success in a novel environment. Ecol. Evol. 8:8043-8054.

Legault, Geoffrey B. 2017. The impacts of demographic stochasticity on populations and communities. PhD diss., University of Colorado at Boulder

Legault G, Bitters ME, Hastings A, Melbourne BA. 2020. Interspecific competition slows range expansion and shapes range boundaries. PNAS 117: 26854-26860.

Melbourne BA, Hastings A 2008. Extinction risk depends strongly on factors contributing to stochasticity. Nature 454(7200):100-103.

Melbourne BA, Hastings A. 2009. Highly variable spread rates in replicated biological invasions: fundamental limits to predictability. Science 325(5947):1536–9

Sokoloff A. 1974. The Biology of Tribolium with special emphasis on genetic aspects. UK: Clarendon Press, Oxford University Press.

Stewart GS, Morris MR, Genis AB, Szűcs M, Melbourne BA, Tavener SJ, Hufbauer RA. 2017. The power of evolutionary rescue is constrained by genetic load. Evol Appl. 10(7):731-741.

Szűcs, M., Melbourne, B.A., Tuff, T., Hufbauer, R.A. 2014. The roles of demography and genetics in the early stages of colonization. Proc. R. Soc. B Biol. Sci. 281, 20141073.

Szűcs M, Melbourne BA, Tuff T, Weiss‐Lehman C, Hufbauer RA. 2017a. Genetic and demographic founder effects have long‐term fitness consequences for colonizing populations. Ecol. Lett. 20:436-444.

Szűcs M, Vahsen ML, Melbourne BA, Hoover C, Weiss-Lehman C, Hufbauer RA. 2017b. Rapid adaptive evolution in novel environments acts as an architect of population range expansion. PNAS 114: 13501-13506.

Vahsen, Megan. 2017. Disentangling drivers of colonization success in laboratory and natural systems. MS thesis, Colorado State University

Vahsen ML., Shea K, Hovis CL, Teller BJ, Hufbauer RA. 2018. Prior adaptation, diversity, and introduction frequency mediate the positive relationship between propagule pressure and the initial success of founding populations. Biol. Invasions 20: 2451-2459.

Van Allen BG., Bhavsar P. 2014. Natal habitat effects drive density dependent scaling of dispersal decisions. Oikos 123(6): 699–704.

Van Allen BG, Rudolf VHW. 2013. Ghosts of habitats past: environmental carry-over effects drive population dynamics in novel habitat. Am. Nat. 181: 596–608.

Van Allen, BG, Rudolf VHW. 2015. Habitat-mediated carry-over effects lead to context-dependent outcomes of species interactions. Journal of Animal Ecology 84(6): 1646-1656.

Van Allen BG, Rudolf VHW. 2016. Carryover effects drive competitive dominance in spatially structured environments. Proc. Natl Acad. Sci. USA 113: 6939–6944.

Weiss-Lehman C, Hufbauer RA, Melbourne BA. 2017. Rapid trait evolution drives increased speed and variance in experimental range expansions. Nature Communications 8: 1-7.