Phenotypic plasticity in response to environmental heterogeneity contributes to fluctuating asymmetry in plants: first empirical evidence

Fluctuating asymmetry (FA) is widely used to quantify developmental instability (DI) in ecological and evolutionary studies. It has long been recognized that FA may not exclusively originate from DI for sessile organisms such as plants, because phenotypic plasticity in response to heterogeneities in the environment might also produce FA. This study provides the first empirical evidence for this hypothesis. We reasoned that solar irradiance, which is greater on the southern side than on the northern side of plants growing in the temperate zone of the Northern Hemisphere, would cause systematic morphological differences and asymmetry associated with the orientation of plant parts. We used geometric morphometrics to characterize the size and shape of flower parts in Iris pumila grown in a common garden. The size of floral organs was not significantly affected by orientation. Shape and particularly its asymmetric component differed significantly according to orientation for three different floral parts. Orientation accounted for 10.4% of the total shape asymmetry within flowers in the falls, for 11.4% in the standards and for 2.2% in the style branches. This indicates that phenotypic plasticity in response to a directed environmental factor, most likely solar irradiance, contributes to FA of flowers under natural conditions. That FA partly results from phenotypic plasticity and not just from DI needs to be considered by studies of FA in plants and other sessile organisms.     

Concordance of bacterial communities of two tick species and blood of their shared rodent host

High‐throughput sequencing is revealing that most macro‐organisms house diverse microbial communities. Of particular interest are disease vectors whose microbiome could potentially affect pathogen transmission and vector competence. We investigated bacterial community composition and diversity of the ticks Dermacentor variabilis (n = 68) and Ixodes scapularis (n = 15) and blood of their shared rodent host, Peromyscus leucopus (n = 45) to quantify bacterial diversity and concordance. The 16S rRNA gene was amplified from genomic DNA from field‐collected tick and rodent blood samples, and 454 pyrosequencing was used to elucidate their bacterial communities. After quality control, over 300 000 sequences were obtained and classified into 118 operational taxonomic units (OTUs, clustered at 97% similarity). Analysis of rarefied communities revealed that the most abundant OTUs were tick species‐specific endosymbionts, Francisella and Rickettsia, and the commonly flea‐associated bacterium Bartonella in rodent blood. An Arsenophonus and additional Francisella endosymbiont were also present in D. variabilis samples. Rickettsia was found in both tick species but not in rodent blood, suggesting that it is not transmitted during feeding. Bartonella was present in larvae and nymphs of both tick species, even those scored as unengorged. Relatively, few OTUs (e.g. Bartonella, Lactobacillus) were found in all sample types. Overall, bacterial communities from each sample type were significantly different and highly structured, independent of their dominant OTUs. Our results point to complex microbial assemblages inhabiting ticks and host blood including infectious agents, tick‐specific endosymbionts and environmental bacteria that could potentially affect arthropod‐vectored disease dynamics.     

Malaria infections reinforce competitive asymmetry between two Ficedula flycatchers in a recent contact zone

Parasites may influence the outcome of interspecific competition between closely related host species through lower parasite virulence in the host with which they share the longer evolutionary history. We tested this idea by comparing the prevalence of avian malaria (Haemosporidia) lineages and their association with survival in pied and collared flycatchers (Ficedula hypoleuca and F. albicollis) breeding in a recent contact zone on the Swedish island of Öland. A nested PCR protocol amplifying haemosporidian fragments of mtDNA was used to screen the presence of malaria lineages in 1048 blood samples collected during 6 years. Competitively inferior pied flycatchers had a higher prevalence of blood parasites, including the lineages that were shared between the two flycatcher species. Multistate mark–recapture models revealed a lower survival of infected versus uninfected female pied flycatchers, while no such effects were detected in male pied flycatchers or in collared flycatchers of either sex. Our results show that a comparatively new host, the collared flycatcher, appears to be less susceptible to a local northern European malarial lineage where the collared flycatchers have recently expanded their distribution. Pied flycatchers experience strong reproductive interference from collared flycatchers, and the additional impact of species‐specific blood parasite effects adds to this competitive exclusion. These results support the idea that parasites can strongly influence the outcome of interspecific competition between closely related host species, but that the invading species need not necessarily be more susceptible to local parasites.     

Development of SNP‐genotyping arrays in two shellfish species

Use of SNPs has been favoured due to their abundance in plant and animal genomes, accompanied by the falling cost and rising throughput capacity for detection and genotyping. Here, we present in vitro (obtained from targeted sequencing) and in silico discovery of SNPs, and the design of medium‐throughput genotyping arrays for two oyster species, the Pacific oyster, Crassostrea gigas, and European flat oyster, Ostrea edulis. Two sets of 384 SNP markers were designed for two Illumina GoldenGate arrays and genotyped on more than 1000 samples for each species. In each case, oyster samples were obtained from wild and selected populations and from three‐generation families segregating for traits of interest in aquaculture. The rate of successfully genotyped polymorphic SNPs was about 60% for each species. Effects of SNP origin and quality on genotyping success (Illumina functionality Score) were analysed and compared with other model and nonmodel species. Furthermore, a simulation was made based on a subset of the C. gigas SNP array with a minor allele frequency of 0.3 and typical crosses used in shellfish hatcheries. This simulation indicated that at least 150 markers were needed to perform an accurate parental assignment. Such panels might provide valuable tools to improve our understanding of the connectivity between wild (and selected) populations and could contribute to future selective breeding programmes.     

Strategic exploitation of fluctuating asymmetry in male Endler's guppy courtship displays is modulated by social environment

Lateral asymmetry in signalling traits enables males to strategically exploit their best side. In many animals, both body colouration and fluctuating asymmetry are signals of male attractiveness. We demonstrated experimentally that even sexually naïve male Poecilia wingei were able to identify their most attractive side (i.e. that with a higher proportion of carotenoid pigmentation) and use it preferentially during courtship. Notably, males retained their strategic signalling in a male‐biased social environment, whereas they ceased to signal strategically in a female‐biased environment. The degree of asymmetry in colouration did not affect overall courtship activity. Strategic lateralization in courtship displays was strongest and most repeatable in the male‐biased social environment where males competed with rivals for matings. Individual asymmetry in colouration changed considerably over a period of 3 months. This suggests that colouration is a dynamic feature during adulthood and that males are capable of tracking and strategically exploiting their lateral asymmetry in accordance with their social environment.     

Morphological adaptations to arboreal habitats and heart position in species of the neotropical whipsnakes genus Chironius

The evolution of arboreality in snakes is accompanied by modifications that are remarkably similar across species. Gravity is one of the most important selective agents, and arboreal snakes present adaptations to circumvent the gradient of pressure, including modifications on heart position (HP) and body slenderness (BS). However, the degree to which different life‐history traits influence the cardiovascular system of snakes remains unclear. Here, we used an ecological and a phylogenetic approach to explore the relationship between habitat, HP, BS, and heart size (HS) in five species of the neotropical whipsnakes genus Chironius that occupy terrestrial, semiarboreal, and arboreal habits. Our ecological comparison indicated that the arboreal species have the most posterior‐positioned heart, the most slender body, and the smallest HS, whereas the terrestrial representative of the group exhibited the most anterior heart, the less flattened body, and the largest HS. After removing the phylogenetic effect, we found no difference in HP and BS between terrestrial and arboreal species. Habitat only differed when contrasting with HS. Body slenderness and HS were correlated with HP. Our results suggest that different restrictions, such as anatomical constraints, behavior, and phylogenetic inertia, may be important for the studied species.     

Divergent habitat use of two urban lizard species

Faunal responses to anthropogenic habitat modification represent an important aspect of global change. In Puerto Rico, two species of arboreal lizard, Anolis cristatellus and A. stratulus, are commonly encountered in urban areas, yet seem to use the urban habitat in different ways. In this study, we quantified differences in habitat use between these two species in an urban setting. For each species, we measured habitat use and preference, and the niche space of each taxon, with respect to manmade features of the urban environment. To measure niche space of these species in an urban environment, we collected data from a total of six urban sites across four different municipalities on the island of Puerto Rico. We quantified relative abundance of both species, their habitat use, and the available habitat in the environment to measure both microhabitat preference in an urban setting, as well as niche partitioning between the two different lizards. Overall, we found that the two species utilize different portions of the urban habitat. Anolis stratulus tends to use more “natural” portions of the urban environment (i.e., trees and other cultivated vegetation), whereas A. cristatellus more frequently uses anthropogenic structures. We also found that aspects of habitat discrimination in urban areas mirror a pattern measured in prior studies for forested sites in which A. stratulus was found to perch higher than A. cristatellus and preferred lower temperatures and greater canopy cover. In our study, we found that the multivariate niche space occupied by A. stratulus did not differ from the available niche space in natural portions of the urban environment and in turn represented a subset of the niche space occupied by A. cristatellus. The unique niche space occupied by A. cristatellus corresponds to manmade aspects of the urban environment generally not utilized by A. stratulus. Our results demonstrate that some species are merely tolerant of urbanization while others utilize urban habitats in novel ways. This finding has implications for long‐term persistence in urban habitats and suggests that loss of natural habitat elements may lead to nonrandom species extirpations as urbanization intensifies.     

Phorid species from Acromyrmex’s hosts and effect on their survival of two fungi proposed for the control of leafcutter ants

Phorid flies (Diptera: Phoridae, Metopinini) are natural enemies of leafcutter ants (Hymenoptera: Formicidae, Attini), which are among the most important pests in the Neotropical region. These parasitoids lay their eggs inside worker ants, causing the death of the parasitized ants, and the oviposition attacks on foraging workers interfere with the collection of vegetal material used in fungal gardens, thereby affecting the whole colony. However, because of the large number of ants per colony, more than one type of biological control agent is needed to have a significant impact. We collected parasitized leafcutter ants Acromyrmex lundii (Guérin‐Méneville), Acromyrmex heyeri (Forel), and Acromyrmex ambiguus (Emery) from various places in Argentina and reared their parasitoids. We recorded developmental times, host and phorid sizes, and other aspects of the biology of the phorids Apocephalus neivai Borgmeier, Apocephalus noetingerorum Brown & Disney, Myrmosicarius gracilipes Borgmeier, Myrmosicarius catharinensis Borgmeier, Myrmosicarius crudelis Borgmeier, and Myrmosicarius cristobalensis Disney et al. This is the first record of A. ambiguus, an important pest of pine plantations, being a host of phorids. We found the first cases of gregarious parasitoidism of a parasitoid with no‐free pupae: M. catharinensis on A. lundii ants. We also evaluated the effect on pupal survival of two cosmopolitan fungi, Beauveria bassiana (Balsamo) Vuill. and Trichoderma lentiforme (Rehm) Chaverri et al., which are also considered as potential biological control agents of leafcutter ants. Suspensions of conidia were tested on Myrmosicarius and Apocephalus parasitoid pupae of different ages. No negative effect on pupal survival was found under either fungal treatment. Therefore, the use of both natural enemies separately but simultaneously, or the introduction of fungi‐inoculated pupae in the pest habitats, seems to be a promising strategy for the multiple biological control of leafcutter ants.     

Relationships between intra‐specific variation in seed size and recruitment in four species in two contrasting habitats

Large seeds contain more stored resources, and seedlings germinating from large seeds generally cope better with environmental stresses such as shading, competition and thick litter layers, than seedlings germinating from small seeds. A pattern with small‐seeded species being associated with open habitats and large‐seeded species being associated with closed (shaded) habitats has been suggested and supported by comparative studies. However, few studies have assessed the intra‐specific relationship between seed size and recruitment, comparing plant communities differing in canopy cover. Here, seeds from four plant species commonly occurring in ecotones between open and closed habitats (Convallaria majalis, Frangula alnus, Prunus padus and Prunus spinosa) were weighed and sown individually (3200 seeds per species) in open and closed‐canopy sites, and seedling emergence and survival recorded over 3 years. Our results show a generally positive, albeit weak, relationship between seed size and recruitment. In only one of the species, C. majalis, was there an association between closed canopy habitat and a positive seed size effect on recruitment. We conclude that there is a weak selection gradient favouring larger seeds, but that this selection gradient is not clearly related to habitat.     

Interspecific interactions influence contrasting spatial genetic structures in two closely related damselfly species

Spatial genetic structure (SGS) is largely determined by colonization history, landscape and ecological characteristics of the species. Therefore, sympatric and ecologically similar species are expected to exhibit similar SGSs, potentially enabling prediction of the SGS of one species from that of another. On the other hand, due to interspecific interactions, ecologically similar species could have different SGSs. We explored the SGSs of the closely related Calopteryx splendens and Calopteryx virgo within Finland and related the genetic patterns to characteristics of the sampling localities. We observed different SGSs for the two species. Genetic differentiation even within short distances in C. splendens suggests genetic drift as an important driver. However, we also observed indication of previous gene flow (revealed by a negative relationship between genetic differentiation and increasing potential connectivity of the landscape). Interestingly, genetic diversity of C. splendens was negatively related to density of C. virgo, suggesting that interspecific interactions influence the SGS of C. splendens. In contrast, genetic differentiation between C. virgo subpopulations was low and only exhibited relationships with latitude, pointing to high gene flow, colonization history and range margin effects as the drivers of SGS. The different SGSs of the two ecologically similar species caution indirect inferences of SGS based on ecologically similar surrogate species.     

Distinct male reproductive strategies in two closely related oak species

Reproductive strategies of closely related species distributed along successional gradients should differ as a consequence of the trade‐off between competition and colonization abilities. We compared male reproductive strategies of Quercus robur and Q. petraea, two partly interfertile European oak species with different successional status. In the studied even‐aged stand, trees of the late‐successional species (Q. petraea) grew faster and suffered less from intertree competition than trees of the early‐successional species (Q. robur). A large‐scale paternity study and a spatially explicit individual‐based mating model were used to estimate parameters of pollen production and dispersal as well as sexual barriers between species. Male fecundity was found to be dependent both on a tree's circumference and on its environment, particularly so for Q. petraea. Pollen dispersal was greater and more isotropic in Q. robur than in Q. petraea. Premating barriers to hybridization were strong in both species, but more so in Q. petraea than in Q. robur. Hence, predictions based on the competition–colonization trade‐off are well supported, whereas the sexual barriers themselves seem to be shaped by colonization dynamics.     

Environmental gradients shape the genetic structure of two medicinal Salvia species in Jordan

• Environmental gradients, and particularly climatic variables, exert a strong influence on plant distribution and, potentially, population genetic diversity and differentiation. Differences in water availability can cause among‐population variation in ecological processes and can thus interrupt populations’ connectivity and isolate them environmentally. The present study examines the effect of environmental heterogeneity on plant populations due to environmental isolation unrelated to geographic distance.
• Using AFLP markers, we analyzed genetic diversity and differentiation among 12 Salvia spinosa populations and 13 Salvia syriaca populations from three phytogeographical regions (Mediterranean, Irano‐Turanian and Saharo‐Arabian) representing the extent of the species’ geographic range in Jordan. Differences in geographic location and climate were considered in the analyses.
• For both species, flowering phenology varied among populations and regions. Irano‐Turanian and Saharo‐Arabian populations had higher genetic diversity than Mediterranean populations, and genetic diversity increased significantly with increasing temperature. Genetic diversity in Salvia syriaca was affected by population size, while genetic diversity responded to drought in S. spinosa. For both species, high levels of genetic differentiation were found as well as two well‐supported phytogeographical groups of populations, with Mediterranean populations clustering in one group and the Irano‐Turanian and Saharo‐Arabian populations in another. Genetic distance was significantly correlated to environmental distance, but not to geographic distance.
• Our data indicate that populations from moist vs. arid environments are environmentally isolated, where environmental gradients affect their flowering phenology, limit gene flow and shape their genetic structure. We conclude that environmental heterogeneity may act as driver for the observed variation in genetic diversity.

     

Contrasting genetic patterns between two coexisting Eleutherococcus species in northern China

Climate oscillations are the key factors to understand the patterns in modern biodiversity. East Asia harbors the most diverse temperate flora, largely because an extensive terrestrial ice cap was absent during repeated Pleistocene glaciation–interglacial cycles. Comparing the demographic histories of species that are codistributed and are close relatives may provide insight into how the process of climate change influences species ranges. In this study, we compared the spatial genetic structure and demographic histories of two coexisting Eleutherococcus species, Eleutherococcus senticosus and E. sessiliflorus. Both species are distributed in northern China, regions that are generally considered to be sensitive to climatic fluctuations. These regions once hosted temperate forest, but this temperate forest was replaced by tundra and taiga forest during the Last Glacial Maximum (LGM), according to pollen records. Using three chloroplast DNA fragments, we assessed the genetic structure of 20 and 9 natural populations of E. senticosus and E. sessiliflorus, respectively. Extremely contrasting genetic patterns were found between the two species; E. sessiliflorus had little genetic variation, whereas E. senticosus had considerably higher levels of genetic variation (15 haplotypes). We speculated that a recent severe bottleneck may have resulted in the extremely low genetic diversity in E. sessiliflorus. In E. senticosus, populations in Northeast China (NEC) harbored all of the haplotypes found in this species and included private haplotypes. The populations in NEC had higher levels of genetic diversity than did those from North China (NC). Therefore, we suggest that both the NC and NEC regions can sustain LGM refugia and that lineage admixture from multiple refugia took place after the LGM elevated the local genetic diversity in NEC. In NEC, multiple genetic hot spots were found in the Changbai Mountains and the Xiaoxing'an Range, which implied that multiple locations in NEC may sustain LGM refugia, even in the Xiaoxing'an Range.     

Response of two parasitoid species (Hymenoptera: Braconidae,Figitidae) to tephritid host and host food substrate cues

The Neotropical‐native figitid Aganaspis pelleranoi (Brèthes) and the Asian braconid Diachasmimorpha longicaudata (Ashmead) are two parasitoids of Tephritidae fruit flies with long and recent, respectively, evolutionary histories in the Neotropics. Both species experienced a recent range of overlap. In Argentina, A. pelleranoi is a potential species in biological control programs against the pestiferous tephritid species, Anastrepha fraterculus (Wiedemann) and Ceratitis capitata (Wiedemann), whereas D. longicaudata is already used in open‐field releases against Medfly in central‐western Argentina. To characterize the host‐foraging strategies of A. pelleranoi and D. longicaudata, olfactometer experiments were conducted comparing responses to C. capitata and A. fraterculus larvae, in two kinds of food substrate: fruit and artificial larval medium. To control the possible influence of host larvae used for parasitoid rearing on olfactory response, two strains of both parasitoid species, reared on both tephrtid species, were studied. Volatiles directly emanating either from A. fraterculus or C. capitata larvae may be detected by both A. pelleranoi and D. longicaudata, although chemical stimuli originating from the combination of host larvae and the habitat of the host were preferred. However, olfactory cues associated with host larvae probably play a relevant role in host searching behaviour of A. pelleranoi, whereas for D. longicaudata, the host‐habitat olfactory stimuli would be highly essential in short‐range host location. The strain of the parasitoids did not affect host search ability on the two tephritid species evaluated. These evidences are relevant for mass production of both parasitoids and their impact following open‐field augmentative releases.     

Behavioral modifications lead to disparate demographic consequences in two sympatric species

Life‐history theory suggests species that typically have a large number of offspring and high adult mortality may make decisions that benefit offspring survival in exchange for increased adult risks. Such behavioral adaptations are essential to understanding how demographic performance is linked to habitat selection during this important life‐history stage. Though studies have illustrated negative fitness consequences to attendant adults or potential fitness benefits to associated offspring because of adaptive habitat selection during brood rearing, equivocal relationships could arise if both aspects of this reproductive trade‐off are not assessed simultaneously. To better understand how adaptive habitat selection during brood rearing influences demographics, we studied the brood survival, attendant parental survival, and space use of two sympatric ground‐nesting bird species, the northern bobwhite (hereafter: “bobwhite”; Colinus virgininanus) and scaled quail (Callipepla squamata). During the 2013–2014 breeding seasons, we estimated habitat suitability across two grains (2 m and 30 m) for both species and determined how adult space use of these areas influenced individual chick survival and parental risk. We found the proportion of a brood's home range containing highly suitable areas significantly increased bobwhite chick survival (β = 0.02, SE = 0.006). Additionally, adult weekly survival for bobwhite was greater for individuals not actively brooding offspring (0.9716, SE = 0.0054) as compared to brooding adults (0.8928, SE = 0.0006). Conversely, brood habitat suitability did not influence scaled quail chick survival during our study, nor did we detect a survival cost for adults that were actively brooding offspring. Our research illustrates the importance of understanding life‐history strategies and how they might influence relationships between adaptive habitat selection and demographic parameters.     

Increased genetic divergence between two closely related fir species in areas of range overlap

Because of introgressive hybridization, closely related species can be more similar to each other in areas of range overlap (parapatry or sympatry) than in areas where they are geographically isolated from each other (allopatry). Here, we report the reverse situation based on nuclear genetic divergence between two fir species, Abies chensiensis and Abies fargesii, in China, at sites where they are parapatric relative to where they are allopatric. We examined genetic divergence across 126 amplified fragment length polymorphism (AFLP) markers in a set of 172 individuals sampled from both allopatric and parapatric populations of the two species. Our analyses demonstrated that AFLP divergence was much greater between the species when comparisons were made between parapatric populations than between allopatric populations. We suggest that selection in parapatry may have largely contributed to this increased divergence.     

Seasonal variation in life history traits in two Drosophila species

Seasonal environmental heterogeneity is cyclic, persistent and geographically widespread. In species that reproduce multiple times annually, environmental changes across seasonal time may create different selection regimes that may shape the population ecology and life history adaptation in these species. Here, we investigate how two closely related species of Drosophila in a temperate orchard respond to environmental changes across seasonal time. Natural populations of Drosophila melanogaster and Drosophila simulans were sampled at four timepoints from June through November to assess seasonal change in fundamental aspects of population dynamics as well as life history traits. D. melanogaster exhibit pronounced change across seasonal time: early in the season, the population is inferred to be uniformly young and potentially represents the early generation following overwintering survivorship. D. melanogaster isofemale lines derived from the early population and reared in a common garden are characterized by high tolerance to a variety of stressors as well as a fast rate of development in the laboratory environment that declines across seasonal time. In contrast, wild D. simulans populations were inferred to be consistently heterogeneous in age distribution across seasonal collections; only starvation tolerance changed predictably over seasonal time in a parallel manner as in D. melanogaster. These results suggest fundamental differences in population and evolutionary dynamics between these two taxa associated with seasonal heterogeneity in environmental parameters and associated selection pressures.     

The effect of close approaches for tagging activities by small research vessels on the behavior of humpback whales (Megaptera novaeangliae)

Small research vessels are often used as platforms for tagging activities to collect behavioral data on cetaceans and they have the potential to disturb that group or individual. If this disturbance is ignored, results and conclusions produced by that study could be inaccurate. Here land‐based behavioral data of migrating humpback whales (Megaptera novaeangliae) (n = 29) were used to determine the effect of close approaches for tagging by research vessels on their diving, movement and surface behaviors. Groups of whales were tagged, using digital recording tags, by small research vessels, as part of a behavioral response study. In groups that were approached for tagging, temporary changes in movement behaviors during close approaches were found, with subsequent recovery to “pre‐approach” levels. In female‐calf groups more long‐term changes in travel speed were found. Results suggest that, although close approaches for tagging by small vessels may cause behavioral changes in humpback whales, this change may be small and temporary. However, in female‐calf groups, the behavioral change may be greater and longer lasting. This study shows that when using small vessels for behavioral research, disturbance, and recovery should be measured to ensure integrity of data used for other analyses.