Dispersal is an important facet of the life history of many organisms and is, therefore, subject to selective pressure but does not evolve in isolation. Across nature, there are examples of dispersal syndromes and life history strategies in which suites of traits coevolve and covary with dispersal in combinations that serve to maximize fitness in a given ecological context. The red rust flour beetle, Tribolium castaneum, is a model organism and globally significant post-harvest pest that relies on dispersal to reach new patches of ephemeral habitat. Dispersal behaviour in Tribolium has a strong genetic basis. However, a robust understanding of the relationship between dispersal and other life-history components, which could elucidate evolutionary processes and allow pest managers to control their spread and reduce the impact of infestation, is currently lacking. Here, we use highly replicated lines of T. castaneum previously artificially selected for divergent small-scale dispersal propensity to robustly test several important life history components: reproductive strategy, development time, and longevity. As predicted, we find that a suite of important changes as a result of our selection on dispersal: high dispersal propensity is associated with a lower number of longer mating attempts by males, lower investment in early life reproduction by females, slower development of later-laid offspring, and longer female life span. These findings indicate that correlated intraspecific variation in dispersal and related traits may represent alternative life history strategies in T. castaneum. We therefore suggest that pest management efforts to mitigate the species' agro-economic impact should consider the eco-evolutionary dynamics within multiple life histories. The benefits of doing so could be felt both through improved targeting of efforts to reduce spread and also in forecasting how the selection pressures applied through pest management are likely to affect pest evolution. Graphical Abstract
Dispersal is an important behavior in many animals, with profound effects on individual fitness and the evolutionary trajectories of populations. This is especially true within taxa with particular life-history strategies, for example those that exploit ephemeral habitat. Further, dispersal is commonly seen to be part of behavioral syndromes - suites of traits that covary across behavioral contexts. The red flour beetle, Tribolium castaneum (Coleoptera, Tenebrionidae), is a major post-harvest crop pest responsible for large losses through the infestation of stored grain. In this system dispersal is known to have a strong genetic basis and differential artificial selection on dispersal traits produces strong phenotypic divergence. However, it is unknown which traits are able to rapidly evolve to produce these results, or which behavioral components underlie differences in dispersal. Using replicate lines of T. castaneum previously selected for divergent dispersal behavior, we test for correlated activity and movement patterns, morphology and substrate surface use. We find robustly repeatable associations between the dispersal phenotype and higher activity, straighter paths, larger body size (but not relative leg length) and increased tendency to remain at the surface of fodder. Together our results suggest that dispersal is part of a syndrome of traits in T. castaneum, and must be treated as such when considering the evolution of dispersal in this system, and in attempting to predict and control its spread.
AbstractSmall, isolated populations are often characterised by low levels of genetic diversity. This can result in inbreeding depression and reduced capacity to adapt to changes in the environment, and therefore higher risk of extinction. However, sometimes these populations can be rescued if allowed to increase in size or if migrants enter, bringing in new allelic variation and thus increasing genetic diversity. This study uses experimental manipulation of population size and migration to quantify their effects on fitness in a challenging environment to better understand genetic rescue. Using small, replicated populations of Tribolium castaneum experimentally evolved to different temperature regimes we tested genetic and demographic rescue, by performing large‐scale manipulations of population size and migration and examining fitness consequences over multiple generations. We measured fitness in high temperature (38°C) thermal lines maintained at their usual ‘small’ population size of N = 100 individuals, and with ‘large’ scaled up duplicates containing N≈10,000 individuals. We compared these large lines with and without migration (m = 0.1) for 10 generations. Additionally, we assessed the effects of outcrossing at an individual level, by comparing fitness of hybrid (thermal line × stock) offspring with within‐line crosses. We found that, at the population level, a rapid increase in the number of individuals in the population resulted in reduced fitness (represented by reproductive output and survival through heatwave conditions), regardless of migration. However, at an individual level, the hybrid offspring of migrants with native individuals generally demonstrated increased longevity in high temperature conditions compared with individuals from thermal selection lines. Overall, these populations showed no evidence that demographic manipulations led to genetic or evolutionary rescue. Following the effects of migration in individuals over several generations may be the next step in unravelling these conflicting results. We discuss these findings in the context of conservation intervention.
The Critically Endangered day gecko Phelsuma antanosy is micro-endemic to 2 humid forest sites in southeastern Madagascar. At one of these, Sainte Luce, it inhabits 4 forest fragments, 2 of which are set to be cleared for mining. Translocation of individuals from within the mining path to protected forest fragments has been proposed to mitigate the impact of habitat loss and the resulting reduction in population size. However, lack of knowledge of its habitat requirements and population structure inhibits efforts to evaluate the likely ecological consequences of translocation. We sampled 92 P. antanosy individuals across each of the known subpopulations in Sainte Luce and assessed the habitat conditions in which they occur, alongside levels of morphological variation. Using 5 morphological trait measures, we found no evidence of subpopulation differentiation. Almost all (>87%) P. antanosy individuals were found on Pandanus longistylus plants and occupancy levels were higher in areas with moderate (30-60%) canopy cover and no other Phelsuma spp. present, suggesting that translocated individuals should be located into these conditions and within a short (<5 m) distance of P. longistylus plants. We propose that siting individuals in patches meeting these criteria may help to maximise translocation efficacy. We discuss our results in the context of the lack of ecological and genetic information on this species, the general need for long-term monitoring of threatened species and the utility of translocation projects to inform and benefit conservation science.
Dispersal behaviour is an important aspect of the life-history of animals. However, the genetic architecture of dispersal-related traits is often obscure or unknown, even in well studied species. Tribolium castaneum is a globally significant post-harvest pest and established model organism, yet studies of its dispersal have shown ambiguous results and the genetic basis of this behaviour remains unresolved. We combine experimental evolution and agent-based modelling to investigate the number of loci underlying dispersal in T. castaneum, and whether the trait is sex-linked. Our findings demonstrate rapid evolution of dispersal behaviour under selection. We find no evidence of sex-biases in the dispersal behaviour of the offspring of crosses, supporting an autosomal genetic basis of the trait. Moreover, simulated data approximates experimental data under simulated scenarios where the dispersal trait is controlled by one or few loci, but not many loci. Levels of dispersal in experimentally inbred lines, compared with simulations, indicate that a single locus model is not well supported. Taken together, these lines of evidence support an oligogenic architecture underlying dispersal in Tribolium castaneum. These results have implications for applied pest management and for our understanding of the evolution of dispersal in the coleoptera, the world's most species-rich order.
Flour beetles of the genus Tribolium have been utilised as informative study systems for over a century and contributed to major advances across many fields. This review serves to highlight the significant historical contribution that Tribolium study systems have made to the fields of ecology and evolution, and to promote their use as contemporary research models. We review the broad range of studies employing Tribolium to make significant advances in ecology and evolution. We show that research using Tribolium beetles has contributed a substantial amount to evolutionary and ecological understanding, especially in the fields of population dynamics, reproduction and sexual selection, population and quantitative genetics, and behaviour, physiology and life history. We propose a number of future research opportunities using Tribolium, with particular focus on how their amenability to forward and reverse genetic manipulation may provide a valuable complement to other insect models.
Abstract Polyandry, when females mate with more than one male, is theorised to play an important role in successful colonisation of new habitats. In addition to possible benefits from sexual selection, even mild polyandry could facilitate colonisation by protecting against inbreeding and reducing the costs of mating with incompatible or infertile males. Here, we measure the importance of mild polyandry for population viability and reproductive fitness following experimental founder events into a higher‐temperature regime. Using colonisation experiments with the model beetle Tribolium castaneum, in which females can produce offspring for up to 140 days following a single mating, we founded more than 100 replicate populations using single females that had been given the opportunity to mate with either one or two males and then tracked their subsequent population dynamics. Following population viability and fitness across 10 generations, we found that extinction rates were significantly lower in populations founded by females given polyandrous opportunities to mate with two males (9%) compared to populations founded by monogamous females (34%). In addition, populations founded by females that had been provided with opportunities to store sperm from two different males showed double the median productivity following colonisation compared to monogamous‐founded populations. Notably, we identified short‐term and longer‐term benefits to post‐colonisation populations from double‐mating, with results suggesting that polyandry acts to both protect against mating with incompatible males through the founder event, and reduce inbreeding depression as the colonisation proceeds for 10 generations. Our results therefore show that even mild polyandry provides both reproductive and genetic benefits for colonising populations.