The origin of a mutualism: a morphological trait promoting the evolution of ant-aphid mutualisms

Mutualisms are mutually beneficial interactions between species and are fundamentally important at all levels of biological organization. It is not clear, however, why one species participates in a particular mutualism whereas another does not. Here we show that pre-existing traits can dispose particular species to evolve a mutualistic interaction. Combining morphological, ecological, and behavioral data in a comparative analysis, we show that resource use in Chaitophorus aphids (Hemiptera: Aphididae) modulates the origin of their mutualism with ants. We demonstrate that aphid species that feed on deeper phloem elements have longer mouthparts, that this inhibits their ability to withdraw their mouthparts and escape predators and that, consequently, this increases their need for protection by mutualist ants.     

Harmonia axyridis invasions: Deducing evolutionary causes and consequences

I consider evolutionary approaches to deducing factors that have made the ladybird beetle Harmonia axyridis such a successful invader, and the contribution that studies of this species in its native range can make. Work aiming to demonstrate which (pre)adaptations have made the species so successful often fails to compare these putative characters with those of other ladybirds. This has led to a tendency for “argument by design”‐type claims on characters widely shared by non‐invasive coccinellids. There is good evidence from genetic studies that evolutionary change occurred in invasive populations, contributing to their success. There is some evidence for subsequent evolutionary change after the establishment of invasive H. axyridis, primarily in the native organisms with which the ladybird interacts. I show here that there appears to have been little adaptation in H. axyridis, over about 20 generations, to the alkaloids of one North American native intraguild prey, the ladybird Coleomegilla maculata. Studies of H. axyridis in its native range are important, as they provide a snapshot of the ancestral ladybird, unobscured by subsequent evolutionary change related to its invasiveness. They provide baseline data about phenomena such as interactions with natural enemies and intraguild predation, and they also can provide pointers as to how H. axyridis might further adapt in the regions it has colonized. Harmonia axyridis represents an ideal opportunity for greater international co‐operation between scientists studying this species in its native range in Asia and scientists studying it in Europe, America and Africa, where it is an invasive exotic.     

EVOLUTIONARY ADAPTATION TO TEMPERATURE. IX. PREADAPTATION TO NOVEL STRESSFUL ENVIRONMENTS OF ESCHERICHIA COLI ADAPTED TO HIGH TEMPERATURE

Abstract Stressful environments may be considered as those that reduce fitness, sometimes due in part to the increased metabolic expenditure required to sustain life. Direct adaptation to a stressor is expected to increase fitness and reduce maintenance metabolism, with the latter leading to increased biomass production. In this study, we test the general hypothesis that such adaptation to one stressor can preadapt organisms to novel stressful environments. Six lines of Escherichia coli propagated for 2000 generations at 41–42°C (42 group), a stressful temperature, were compared to six control lines propagated for 2000 generations at 37°C (37 group) and to the common ancestor of both groups. We assayed biovolume yield (a measure of growth efficiency) and competitive fitness in the 42 group's selective high temperature environment as well as five novel stressful environments–acid, alkali, ethanol, high osmolarity and peroxide. As previously reported, at high temperature the 42 group had both higher yield and fitness than the 37 group and ancestor. In the novel environments, the 42 group generally produced yields higher than the 37 group (and marginally higher than the ancestor), but we found no differences in competitive fitness among the 37 and 42 groups and the ancestor. We also found that the performance of lines within groups was not correlated across stressful environments for either yield or relative fitness. Because previous adaptation to one stressor did not improve our measure of Darwinian fitness in novel stressful environments, we conclude that the 42 group shows no useful preadaptation, or cross‐tolerance, to these types of environments.     

Genomic signatures of rapid adaptive evolution in the bluespotted cornetfish,a Mediterranean Lessepsian invader

Biological invasions are increasingly creating ecological and economical problems both on land and in aquatic environments. For over a century, the Mediterranean Sea has steadily been invaded by Indian Ocean/Red Sea species (called Lessepsian invaders) via the Suez Canal, with a current estimate of ~450 species. The bluespotted cornetfish, Fistularia commersonii, considered a ‘Lessepsian sprinter’, entered the Mediterranean in 2000 and by 2007 had spread through the entire basin from Israel to Spain. The situation is unique and interesting both because of its unprecedented rapidity and by the fact that it took this species c. 130 years to immigrate into the Mediterranean. Using genome scans, with restriction site‐associated DNA (RAD) sequencing, we evaluated neutral and selected genomic regions for Mediterranean vs. Red Sea cornetfish individuals. We found that few fixed neutral changes were detectable among populations. However, almost half of the genes associated with the 47 outlier loci (potentially under selection) were related to disease resistance and osmoregulation. Due to the short time elapsed from the beginning of the invasion to our sampling, we interpret these changes as signatures of rapid adaptation that may be explained by several mechanisms including preadaptation and strong local selection. Such genomic regions are therefore good candidates to further study their role in invasion success.     

Two intromittent organs in Zorotypus caudelli (Insecta,Zoraptera): the paradoxical coexistence of an extremely long tube and a large spermatophore

Very unusual genitalia of the species Zorotypus caudelli are described. It contains the unique configuration of two different intromittent organs, one of them strongly elongated. Hyper elongated genitalia are known in different groups of insects. Males have to accommodate these unwieldy structures in the limited spaces of the abdomen and manipulate them acutely during copulation. A crucial question is how do species with elongated genitalia cope with these requirements? To investigate this, we studied key features enabling storage, insertion, and withdrawal of the elongated genitalia. The co‐existence of an elongated narrow tube and a bulky spermatophore is a highly unusual and apparently paradoxical condition. However, we demonstrate that the tube is not involved in sperm transmission, whereas the large spermatophore is transferred to females by a membranous fold of the genitalia. The movement of the spermatophore is caused by haemolymph pressure, which likely also promotes the insertion of both intromittent organs. A comparison with the genital anatomy and reproductive mode in related groups suggests that the elongated tube and its accommodating pouch is a de novo structure, and that the ancestral sperm transport via spermatophore is a preadaptive condition for the acquisition of this unusual structure. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 40–54.     

Mosaic evolution,preadaptation, and the evolution of evolvability in apes

A major goal in postsynthesis evolutionary biology has been to better understand how complex interactions between traits drive movement along and facilitate the formation of distinct evolutionary pathways. I present analyses of a character matrix sampled across the haplorrhine skeleton that revealed several modules of characters displaying distinct patterns in macroevolutionary disparity. Comparison of these patterns to those in neurological development showed that early ape evolution was characterized by an intense regime of evolutionary and developmental flexibility. Shifting and reduced constraint in apes was met with episodic bursts in phenotypic innovation that built a wide array of functional diversity over a foundation of shared developmental and anatomical structure. Shifts in modularity drove dramatic evolutionary changes across the ape body plan in two distinct ways: (1) an episode of relaxed integration early in hominoid evolution coincided with bursts in evolutionary rate across multiple character suites; (2) the formation of two new trait modules along the branch leading to chimps and humans preceded rapid and dramatic evolutionary shifts in the carpus and pelvis. Changes to the structure of evolutionary mosaicism may correspond to enhanced evolvability that has a “preadaptive” effect by catalyzing later episodes of dramatic morphological remodeling.     

Habitat-dependent thermal regimes of two hawaiian geckos (Reptilla: gekkonidae)

1. 1.Effects of habitat on the thermal regime were investigated in two diurno—nocturnal geckos in Hawaii.

2. 2.In trees Hemidactylus frenatus thermoregulated in daytime with body temperature (BT) above air temperture (AT); in houses some thermoregulated likewise in daytime but mainly the species thermoregulated at night, on electric lamps, to the same BT as in trees by day.

3. 3.Lepidodactylus lugubris in trees thermoregulated in daytime, its BT lower than in H. frenatus. In the rocks it had at night a BT resembling that in trees in daytime, because the thermal cycle in rock crevices lagged behind outside AT.

4. 4.The flexibility of these geckos in thermal regime and activity cycle preadapts them to both migration and invasion of houses.

EVOLUTIONARY ADAPTATION TO TEMPERATURE. V. ADAPTIVE MECHANISMS AND CORRELATED RESPONSES IN EXPERIMENTAL LINES OF ESCHERICHIA COLI

We previously demonstrated temperature-specific genetic adaptation in experimental lines of Escherichia coli. Six initially identical populations were propagated for 2000 generations under each of five regimes: constant 20°C, 32°C, 37°C, and 42°C, and a daily switch between 32°C and 42°C. Glucose was the sole carbon source in all cases. Here, we examine the physiological bases of adaptation to determine whether the same mechanisms evolved among the replicate lines within each thermal regime and across different regimes. Specifically, we investigate whether changes in glucose transport may account for the temperature-specific adaptation. We compared each line's direct response of fitness to glucose with its correlated response to maltose; glucose and maltose enter the cell by different pathways, but their catabolism is identical. Except for lines maintained at the ancestral temperature (37°C), almost all derived lines had significantly different fitnesses (relative to their common ancestor) in glucose and maltose, supporting the hypothesis that adaptation involved changes in glucose transport. An alternative explanation, that maltose transport decayed by genetic drift, appears unlikely for reasons that are discussed. Although most lines showed evidence of temperature-specific adaptation in glucose transport, several different mechanisms may underlie these improvements, as indicated by heterogeneity in correlated responses (across temperatures and substrates) among replicate lines adapted to the same regime. This heterogeneity provides a latent pool of genetic variation for responding to environmental change.     

Arthropod body-plan evolution in the Cambrian with an example from anomalocaridid muscle

The ancestor of the arthropods is widely thought to have possessed a hydrostatic skeleton surrounded by peripheral longitudinal and circular musculature, as exhibited by the extant onychophorans. However, the transition to a lever-style musculature system with an articulating exoskeleton poses a difficult problem in functional evolution: did the musculature or the exoskeleton evolve first, and how? Here, by reference to the musculature of the Lower Cambrian stem-group arthropod Pambdelurion, the problem is resolved in terms of preadaptation and functional degeneracy without recourse to saltational notions. Cambrian taxa lying in the stem-groups of the modern phyla may thus be shown to provide unique evidence for the functional progression involved in the assembly of the extant body plans and obviate the need for exotic genetic or developmental mechanisms to explain the evolution of integrated and complex body plans. The notion of the phylum representing a particularly significant level of organization is thereby brought into question.     

The role of preadaptation,propagule pressure and competition in the colonization of new habitats

To successfully colonize new habitats, organisms not only need to gain access to it, they also need to cope with the selective pressures imposed by the local biotic and abiotic conditions. The number of immigrants, the preadaptation to the local habitat and the presence of competitors are important factors determining the success of colonization. Here, using two experimental set-ups, we studied the effect of interspecific competition in combination with propagule pressure and preadaptation on the colonization success of new habitats. Our model system consisted of tomato plants (the novel habitat), the two-spotted spider mite Tetranychus urticae as our focal species and the red spider mite Tetranychus evansi as a competitor. Our results show that propagule pressure and preadaptation positively affect colonization success. More successful populations reach larger final population sizes either by having higher per capita growth rates (due to preadaptation effects) or by starting a population with a larger number of individuals. Although populations are more successful colonizing non-competitive environments than competitive ones, propagule pressure and preadaptation counteract the negative effects of competition, promoting colonization success. Our study shows the importance of propagule pressure and preadaptation for successful colonization of new habitats by providing the ability to cope with both the exigencies of new environments and the community context.