A life‐cycle approach to species barriers

What maintains reproductive barriers between closely related species is, of course, of fundamental interest to a closer understanding of the mechanisms that generate new biodiversity. One important dichotomy is to separate barriers evolved from divergent selection over environmental gradients (extrinsic barriers) from barriers caused by incompatibilities between different genetic arrangements that may have evolved in isolation (intrinsic barriers). This dichotomy also reflects an important applied consequence. As the extrinsic barriers are associated with specific environmental contexts, they may be partly or completely erased if the environment changes. In contrast, intrinsic barriers are inert to the environmental context and resistant to environmental changes. From a conservation biology perspective, it may thus be important to be able to separate extrinsic and intrinsic species barriers, but this may in many organisms be a complex matter. In this issue of Molecular Ecology, Montecinos et al. ( 2017 ) found a tractable approach that works for species with life cycles that include two reproductive but ecologically similar generations, one haploid and the other diploid. What they demonstrate is that using a life‐cycle approach offers a unique possibility to separate between prezygotic and postzygotic barriers. Indeed, in the case of an isomorphic life cycle, there is even a possibility to suggest whether postzygotic barriers are more likely to be intrinsic or extrinsic. In this way, their approach may be useful both to increase our understanding of the basic mechanisms of speciation and to single out when species barriers will better resist environmental changes.     

Species divergence in field crickets: genetics,song, ecomorphology,and pre‐ and postzygotic isolation

Studies that simultaneously estimate levels of species divergence in genetics, reproductive and ecological traits, and pre‐ and postzygotic isolation are relatively rare. Here we compare levels of divergence in three allopatric sister species of field crickets. We compare divergence in both nuclear and mitochondrial DNA, male song, female ovipositor length, levels of pre‐ and postzygotic isolation, and male versus female contributions to prezygotic isolation. Taken together, our data show the accumulation of a multitude of potential reproductive isolating barriers if secondary contact were to become established. Furthermore, ecological and behavioural prezygotic isolation appear significantly more advanced than postzygotic isolation, with prezygotic isolation due to female behaviour exceeding that due to male behaviour.     

Impact of pre‐ and post‐pollination barriers on pollen transfer and reproductive isolation among three sympatric Pedicularis (Orobanchaceae) species

• Pedicularis is the largest genus in the Orobanchaceae (>300) with many species co‐occurring and co‐blooming in subalpine to alpine meadows in the Himalayas. Although it is well known that different Pedicularis species place pollen on different parts of the same bumblebee's body, thus reducing interspecific pollen transfer, it is not known whether post‐pollination components also contribute to reproductive isolation (RI).
• In this study, we quantified the individual strengths and absolute contributions of six pre‐ and post‐pollination components of RI between three sympatric species in two pairs; Pedicularis gruina × Pedicularis tenuisecta (gru × ten) and Pedicularis comptoniifolia × Pedicularis tenuisecta (com × ten).
• All three Pedicularis species shared the same Bombus species. Individual foragers showed a high, but incomplete, floral constancy for each species. Therefore, pre‐pollination barriers were potentially ‘leaky’ as Bombus species showed a low but consistent frequency of interspecific visitation. The RI strength of pre‐pollination was lower in com × ten than in gru × ten. In contrast, post‐pollination barriers completely blocked gene flow between both sets of species pairs. Two post‐pollination recognition sites were identified. Late acting rejection of interspecific pollen tube growth occurred in com♀ × ten♂, while seeds produced in bi‐directional crosses of gru × ten failed to germinate.
• We propose that, although floral isolation based on pollen placement on pollinators in the genus Pedicularis is crucial to avoid interspecific pollen transfer, the importance of this mode of interspecific isolation may be exaggerated. Post‐pollination barriers may play even larger roles for currently established populations of co‐blooming and sympatric species in this huge genus in the Himalayas.

     

Invasion of novel habitats uncouples haplo‐diplontic life cycles

Baker's Law predicts uniparental reproduction will facilitate colonization success in novel habitats. While evidence supports this prediction among colonizing plants and animals, few studies have investigated shifts in reproductive mode in haplo‐diplontic species in which both prolonged haploid and diploid stages separate meiosis and fertilization in time and space. Due to this separation, asexual reproduction can yield the dominance of one of the ploidy stages in colonizing populations. We tested for shifts in ploidy and reproductive mode across native and introduced populations of the red seaweed Gracilaria vermiculophylla. Native populations in the northwest Pacific Ocean were nearly always attached by holdfasts to hard substrata and, as is characteristic of the genus, haploid–diploid ratios were slightly diploid‐biased. In contrast, along North American and European coastlines, introduced populations nearly always floated atop soft‐sediment mudflats and were overwhelmingly dominated by diploid thalli without holdfasts. Introduced populations exhibited population genetic signals consistent with extensive vegetative fragmentation, while native populations did not. Thus, the ecological shift from attached to unattached thalli, ostensibly necessitated by the invasion of soft‐sediment habitats, correlated with shifts from sexual to asexual reproduction and slight to strong diploid bias. We extend Baker's Law by predicting other colonizing haplo‐diplontic species will show similar increases in asexuality that correlate with the dominance of one ploidy stage. Labile mating systems likely facilitate colonization success and subsequent range expansion, but for haplo‐diplontic species, the long‐term eco‐evolutionary impacts will depend on which ploidy stage is lost and the degree to which asexual reproduction is canalized.     

Differences in developmental strategies between long‐settled and invasion‐front populations of the cane toad in Australia

Phenotypic plasticity can enhance a species’ ability to persist in a new and stressful environment, so that reaction norms are expected to evolve as organisms encounter novel environments. Biological invasions provide a robust system to investigate such changes. We measured the rates of early growth and development in tadpoles of invasive cane toads (Rhinella marina) in Australia, from a range of locations and at different larval densities. Populations in long‐colonized areas have had the opportunity to adapt to local conditions, whereas at the expanding range edge, the invader is likely to encounter challenges that are both novel and unpredictable. We thus expected invasion‐vanguard populations to exhibit less phenotypic plasticity than range‐core populations. Compared to clutches from long‐colonized areas, clutches from the invasion front were indeed less plastic (i.e. rates of larval growth and development were less sensitive to density). In contrast, those rates were highly variable in clutches from the invasion front, even among siblings from the same clutch under standard conditions. Clutches with highly variable rates of growth and development under constant conditions had lower phenotypic plasticity, suggesting a trade‐off between these two strategies. Although these results reveal a strong pattern, further investigation is needed to determine whether these different developmental strategies are adaptive (i.e. adaptive phenotypic plasticity vs. bet‐hedging) or instead are driven by geographic variation in genetic quality or parental effects.     

Late‐onset progressive retinal atrophy in the Gordon and Irish Setter breeds is associated with a frameshift mutation in C2orf71

Progressive retinal atrophy (PRA) in dogs is characterised by the degeneration of the photoreceptor cells of the retina, resulting in vision loss and eventually complete blindness. The condition affects more than 100 dog breeds and is known to be genetically heterogeneous between breeds. Around 14 mutations have now been identified that are associated with PRA in around 49 breeds, but for the majority of breeds the mutation(s) responsible have yet to be identified. Using genome‐wide association with 16 Gordon Setter PRA cases and 22 controls, we identified a novel PRA locus, termed rod–cone degeneration 4 (rcd4), on CFA17 (P_raw = 2.22 × 10^?8, P_genome = 2.00 × 10^?5), where a 3.2‐Mb region was homozygous within cases. A frameshift mutation was identified in C2orf71, a gene located within this region. This variant was homozygous in 19 of 21 PRA cases and was at a frequency of approximately 0.37 in the Gordon Setter population. Approximately 10% of cases in our study (2 of 21) are not associated with this C2orf71 mutation, indicating that PRA in this breed is genetically heterogeneous and caused by at least two mutations. This variant is also present in a number of Irish Setter dogs with PRA and has an estimated allele frequency of 0.26 in the breed. The function of C2orf71 remains unknown, but it is important for retinal development and function and has previously been associated with autosomal recessive retinitis pigmentosa in humans.     

A cryptic contact zone between divergent mitochondrial DNA lineages in southwestern North America supports past introgressive hybridization in the yellow‐rumped warbler complex (Aves: Dendroica coronata)

Using genetic data to study the process of population divergence is central to understanding speciation, yet distinguishing between recent divergence and introgressive hybridization is challenging. In a previous study on the phylogeography of the yellow‐rumped warbler complex using mitochondrial (mt)DNA data, we reported limited sequence divergence and a lack of reciprocal monophyly between myrtle and Audubon's warblers (Dendroica coronata and Dendroica auduboni, respectively), suggesting very recent isolation. In the present study, we report the results obtained from a subsequent sampling of Audubon's warbler in Arizona and Utah (‘memorabilis’ race), which shows that, although this taxon is similar to auduboni in plumage colour, most memorabilis individuals sampled (93%) carry haplotypes that belong to the divergent black‐fronted warbler lineage (Dendroica nigrifrons) of Mexico. Furthermore, the auduboni and nigrifrons lineages mix in southern Utah at a narrow, yet apparently ‘cryptic’ contact zone. Newly‐available evidence from nuclear markers indicating marked differentiation between auduboni and coronata has focused attention on the possibility of mtDNA introgression in the absence of nuclear gene flow, and the results of the present study are consistent with the hypothesis that the mtDNA of auduboni was indeed historically introgressed from the coronata lineage. Analysis of morphological traits shows that memorabilis is significantly differentiated from auduboni and nigrifrons in some traits, yet is overall intermediate between the two, which is consistent with a shared common ancestor for the auduboni/memorabilis/nigrifrons group. The striking, unexpected mtDNA pattern reported in the present study reveals a complex evolutionary history of the yellow‐rumped warbler complex, and cautions against the exclusive use of mtDNA to infer evolutionary relationships. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 696–706.     

Optimizing the trade‐off between spatial and genetic sampling efforts in patchy populations: towards a better assessment of functional connectivity using an individual‐based sampling scheme

Genetic data are increasingly used in landscape ecology for the indirect assessment of functional connectivity, that is, the permeability of landscape to movements of organisms. Among available tools, matrix correlation analyses (e.g. Mantel tests or mixed models) are commonly used to test for the relationship between pairwise genetic distances and movement costs incurred by dispersing individuals. When organisms are spatially clustered, a population‐based sampling scheme (PSS) is usually performed, so that a large number of genotypes can be used to compute pairwise genetic distances on the basis of allelic frequencies. Because of financial constraints, this kind of sampling scheme implies a drastic reduction in the number of sampled aggregates, thereby reducing sampling coverage at the landscape level. We used matrix correlation analyses on simulated and empirical genetic data sets to investigate the efficiency of an individual‐based sampling scheme (ISS) in detecting isolation‐by‐distance and isolation‐by‐barrier patterns. Provided that pseudo‐replication issues are taken into account (e.g. through restricted permutations in Mantel tests), we showed that the use of interindividual measures of genotypic dissimilarity may efficiently replace interpopulation measures of genetic differentiation: the sampling of only three or four individuals per aggregate may be sufficient to efficiently detect specific genetic patterns in most situations. The ISS proved to be a promising methodological alternative to the more conventional PSS, offering much flexibility in the spatial design of sampling schemes and ensuring an optimal representativeness of landscape heterogeneity in data, with few aggregates left unsampled. Each strategy offering specific advantages, a combined use of both sampling schemes is discussed.     

ScRALF3, a secreted RALF‐like peptide involved in cell–cell communication between the sporophyte and the female gametophyte in a solanaceous species

Small peptides have been shown to regulate numerous aspects of plant development through cell–cell communication. These signaling events are particularly important during reproduction, regulating gamete development and embryogenesis. Rapid alkalinization factor (RALF)‐like genes, a large gene family that encodes secreted peptides, have specific or ubiquitous expression patterns. Previously, five RALF‐like genes with potential involvement during reproduction were isolated from Solanum chacoense. Here, we show that ScRALF3 is an important peptide regulator of female gametophyte development. Its expression, which is auxin‐inducible, is strictly regulated before and after fertilization. Down‐regulation of ScRALF3 expression by RNA interference leads to the production of smaller fruits that produce fewer seeds, due to improper development of the embryo sacs. Defects include loss of embryo sac nuclei polarization, as well as an increase in asynchronous division, accounting for cellular dysfunctions and premature embryo sac development arrest during megagametogenesis. ScRALF3 is expressed in the sporophytic tissue surrounding the embryo sac, the integument and the nucellus, as revealed by in situ hybridization and GUS staining. As expected for a secreted peptide, fluorescence from an ScRALF3–GFP fusion construct is detected throughout the secretory pathway. Therefore, the ScRALF3 secreted peptide may be directly involved in the regulation of multiple aspects of cell–cell communication between the female gametophyte and its surrounding sporophytic tissue during ovule development.     

r‐ and K‐selection in fluctuating populations is determined by the evolutionary trade‐off between two fitness measures: Growth rate and lifetime reproductive success

In a stable environment, evolution maximizes growth rates in populations that are not density regulated and the carrying capacity in the case of density regulation. In a fluctuating environment, evolution maximizes a function of growth rate, carrying capacity and environmental variance, tending to r‐selection and K‐selection under large and small environmental noise, respectively. Here we analyze a model in which birth and death rates depend on density through the same function but with independent strength of density dependence. As a special case, both functions may be linear, corresponding to logistic dynamics. It is shown that evolution maximizes a function of the deterministic growth rate r₀ and the lifetime reproductive success (LRS) R₀, both defined at small densities, as well as the environmental variance. Under large noise this function is dominated by r₀ and average lifetimes are small, whereas R₀ dominates and lifetimes are larger under small noise. Thus, K‐selection is closely linked to selection for large R₀ so that evolution tends to maximize LRS in a stable environment. Consequently, different quantities (r₀ and R₀) tend to be maximized at low and high densities, respectively, favoring density‐dependent changes in the optimal life history.     

Gimme shelter – the relative sensitivity of parasitic nematodes with direct and indirect life cycles to climate change

Climate change is expected to alter the dynamics of host–parasite systems globally. One key element in developing predictive models for these impacts is the life cycle of the parasite. It is, for example, commonly assumed that parasites with an indirect life cycle would be more sensitive to changing environmental conditions than parasites with a direct life cycle due to the greater chance that at least one of their obligate host species will go extinct. Here, we challenge this notion by contrasting parasitic nematodes with a direct life cycle against those with an indirect life cycle. Specifically, we suggest that behavioral thermoregulation by the intermediate host may buffer the larvae of indirectly transmitted parasites against temperature extremes, and hence climate warming. We term this the ‘shelter effect’. Formalizing each life cycle in a comprehensive model reveals a fitness advantage for the direct life cycle over the indirect life cycle at low temperatures, but the shelter effect reverses this advantage at high temperatures. When examined for seasonal environments, the models suggest that climate warming may in some regions create a temporal niche in mid‐summer that excludes parasites with a direct life cycle, but allows parasites with an indirect life cycle to persist. These patterns are amplified if parasite larvae are able to manipulate their intermediate host to increase ingestion probability by definite hosts. Furthermore, our results suggest that exploiting the benefits of host sheltering may have aided the evolution of indirect life cycles. Our modeling framework utilizes the Metabolic Theory of Ecology to synthesize the complexities of host behavioral thermoregulation and its impacts on various temperature‐dependent parasite life history components in a single measure of fitness, R₀. It allows quantitative predictions of climate change impacts, and is easily generalized to many host–parasite systems.     

Contrasting responses to Pleistocene climate changes: a case study of two sister species Allium cyathophorum and A. spicata (Amaryllidaceae) distributed in the eastern and western Qinghai–Tibet Plateau

It has been hypothesized that species occurring in the eastern and the western Qinghai–Tibet Plateau (QTP) responded differently to climate changes during the Pleistocene. Here, we test this hypothesis by phylogeographic analysis of two sister species, Allium cyathophorum and A. spicata. We sequenced two chloroplast DNA (cpDNA) fragments (accD‐psaI and the rpl16 intron) of 150 individuals, and the nuclear (ITS) region of 114 individuals, from 19 populations throughout the distributional ranges of these species. The divergence between the two species was dated at 779 ‐ 714 thousand years before the present and was likely initiated by the most major glaciation in the QTP. Analysis of chlorotype diversity showed that A. spicata, the species occurring in the western QTP, contains much lower genetic diversity (0.25) than A. cyathophorum (0.93), which is distributed in the eastern QTP. Moreover, multiple independent tests suggested that the A. spicata population had expanded recently, while no such expansion was detected in A. cyathophorum, indicating a contrasting pattern of responses to Pleistocene climate changes. These findings highlight the importance of geographical topography in determining how species responded to the climate changes that took place in the QTP during the Pleistocene.     

Future warmer seas: increased stress and susceptibility to grazing in seedlings of a marine habitat‐forming species

Increases in seawater temperature are expected to have negative consequences for marine organisms. Beyond individual effects, species‐specific differences in thermal tolerance are predicted to modify species interactions and increase the strength of top‐down effects, particularly in plant–herbivore interactions. Shifts in trophic interactions will be especially important when affecting habitat‐forming species such as seagrasses, as the consequences on their abundance will cascade throughout the food web. Seagrasses are a major component of coastal ecosystems offering important ecosystem services, but are threatened by multiple anthropogenic stressors, including warming. The mechanistic understanding of seagrass responses to warming at multiple scales of organization remains largely unexplored, especially in early‐life stages such as seedlings. Yet, these early‐life stages are critical for seagrass expansion processes and adaptation to climate change. In this study, we determined the effects of a 3 month experimental exposure to present and predicted mean summer SST of the Mediterranean Sea (25°C, 27°C, and 29°C) on the photophysiology, size, and ecology (i.e., plant‐herbivore interactions) of seedlings of the seagrass Posidonia oceanica. Warming resulted in increased mortality, leaf necrosis, and respiration as well as lower carbohydrate reserves in the seed, the main storage organ in seedlings. Aboveground biomass and root growth were also limited with warming, which could hamper seedling establishment success. Furthermore, warming increased the susceptibility to consumption by grazers, likely due to lower leaf fiber content and thickness. Our results indicate that warming will negatively affect seagrass seedlings through multiple direct and indirect pathways: increased stress, reduced establishment potential, lower storage of carbohydrate reserves, and increased susceptibly to consumption. This work provides a significant step forward in understanding the major mechanisms that will drive the capacity of seagrass seedlings to adapt and survive to warming, highlighting the potential additive effects that herbivory will have on ultimately determining seedling success.     

Geographic variation in seed traits within and among forty‐two species of Rhododendron (Ericaceae) on the Tibetan plateau: relationships with altitude,habitat, plant height,and phylogeny

Seed mass and morphology are plant life history traits that influence seed dispersal ability, seeding establishment success, and population distribution pattern. Southeastern Tibet is a diversity center for Rhododendron species, which are distributed from a few hundred meters to 5500 m above sea level. We examined intra‐ and interspecific variation in seed mass and morphology in relation to altitude, habitat, plant height, and phylogeny. Seed mass decreased significantly with the increasing altitude and increased significantly with increasing plant height among populations of the same species. Seed mass differed significantly among species and subsections, but not among sections and subgenera. Seed length, width, surface area, and wing length were significantly negative correlated with altitude and significantly positive correlated with plant height. Further, these traits differed significantly among habitats and varied among species and subsection, but not among sections and subgenera. Species at low elevation had larger seeds with larger wings, and seeds became smaller and the wings of seeds tended to be smaller with the increasing altitude. Morphology of the seed varied from flat round to long cylindrical with increasing altitude. We suggest that seed mass and morphology have evolved as a result of both long‐term adaptation and constraints of the taxonomic group over their long evolutionary history.