The resolution of evolutionary conflicts within species.

Evolutionary conflicts of interest occur at all levels, scales and forms of biological organization. They are a fundamental component of the living world and range from conflicts between genetic elements and cells, to conflicts between the sexes and between competing individuals. Yet, the existence of admirably well functioning genomes, bodies, mating pairs and societies suggests that processes must exist to resolve or mitigate such conflicts. We organized this special feature 'The resolution of evolutionary conflicts within species' to encourage the flow of knowledge between fields that traditionally have often taken different approaches to study evolutionary conflicts. Contributed papers discuss data from bacteria, plants and animals (including humans) and present theory, molecular mechanisms and population dynamics of how conflicts are resolved in nature. Together, they contribute to a synthetic theory of conflict resolution.

Ecology, the pace-of-life, epistatic selection and the maintenance of genetic variation in life-history genes.

Evolutionary genetics has long struggled with understanding how functional genes under selection remain polymorphic in natural populations. Taking as a starting point that natural selection is ultimately a manifestation of ecological processes, we spotlight an underemphasized and potentially ubiquitous ecological effect that may have fundamental effects on the maintenance of genetic variation. Negative frequency dependency is a well-established emergent property of density dependence in ecology, because the relative profitability of different modes of exploiting or utilizing limiting resources tends to be inversely proportional to their frequency in a population. We suggest that this may often generate negative frequency-dependent selection (NFDS) on major effect loci that affect rate-dependent physiological processes, such as metabolic rate, that are phenotypically manifested as polymorphism in pace-of-life syndromes. When such a locus under NFDS shows stable intermediate frequency polymorphism, this should generate epistatic selection potentially involving large numbers of loci with more minor effects on life-history (LH) traits. When alternative alleles at such loci show sign epistasis with a major effect locus, this associative NFDS will promote the maintenance of polygenic variation in LH genes. We provide examples of the kind of major effect loci that could be involved and suggest empirical avenues that may better inform us on the importance and reach of this process.

Condition dependence and the paradox of missing plasticity costs.

Phenotypic plasticity plays a key role in adaptation to changing environments. However, plasticity is neither perfect nor ubiquitous, implying that fitness costs may limit the evolution of phenotypic plasticity in nature. The measurement of such costs of plasticity has proved elusive; decades of experiments show that fitness costs of plasticity are often weak or nonexistent. Here, we show that this paradox could potentially be explained by condition dependence. We develop two models differing in their assumptions about how condition dependence arises; both models show that variation in condition can readily mask costs of plasticity even when such costs are substantial. This can be shown simply in a model where plasticity itself evolves condition dependence, which would be expected if costly. Yet similar effects emerge from an alternative model where trait expression itself is condition-dependent. In this more complex model, the average condition in each environment and genetic covariance in condition across environments both determine when costs of plasticity can be revealed. Analogous to the paradox of missing trade-offs between life history traits, our models show that variation in condition can mask costs of plasticity even when costs exist, and suggest this conclusion may be robust to the details of how condition affects trait expression. Our models suggest that condition dependence can also account for the often-observed pattern of elevated plasticity costs inferred in stressful environments, the maintenance of genetic variance in plasticity, and provides insight into experimental and biological scenarios ideal for revealing a cost of phenotypic plasticity.

Transcriptome-based Phylogeny of the Semi-aquatic Bugs (Hemiptera: Heteroptera: Gerromorpha) Reveals Patterns of Lineage Expansion in a Series of New Adaptive Zones.

Key innovations enable access to new adaptive zones and are often linked to increased species diversification. As such, innovations have attracted much attention, yet their concrete consequences on the subsequent evolutionary trajectory and diversification of the bearing lineages remain unclear. Water striders and relatives (Hemiptera: Heteroptera: Gerromorpha) represent a monophyletic lineage of insects that transitioned to live on the water-air interface and that diversified to occupy ponds, puddles, streams, mangroves and even oceans. This lineage offers an excellent model to study the patterns and processes underlying species diversification following the conquest of new adaptive zones. However, such studies require a reliable and comprehensive phylogeny of the infraorder. Based on whole transcriptomic datasets of 97 species and fossil records, we reconstructed a new phylogeny of the Gerromorpha that resolved inconsistencies and uncovered strong support for previously unknown relationships between some important taxa. We then used this phylogeny to reconstruct the ancestral state of a set of adaptations associated with water surface invasion (fluid locomotion, dispersal and transition to saline waters) and sexual dimorphism. Our results uncovered important patterns and dynamics of phenotypic evolution, revealing how the initial event of water surface invasion enabled multiple subsequent transitions to new adaptive zones on the water surfaces. This phylogeny and the associated transcriptomic datasets constitute highly valuable resources, making Gerromorpha an attractive model lineage to study phenotypic evolution.

Direct and indirect effects of male genital elaboration in female seed beetles.

Our understanding of coevolution between male genitalia and female traits remains incomplete. This is perhaps especially true for genital traits that cause internal injuries in females, such as the spiny genitalia of seed beetles where males with relatively long spines enjoy a high relative fertilization success. We report on a new set of experiments, based on extant selection lines, aimed at assessing the effects of long male spines on females in Callosobruchus maculatus. We first draw on an earlier study using microscale laser surgery, and demonstrate that genital spines have a direct negative (sexually antagonistic) effect on female fecundity. We then ask whether artificial selection for long versus short spines resulted in direct or indirect effects on female lifetime offspring production. Reference females mating with males from long-spine lines had higher offspring production, presumably due to an elevated allocation in males to those ejaculate components that are beneficial to females. Remarkably, selection for long male genital spines also resulted in an evolutionary increase in female offspring production as a correlated response. Our findings thus suggest that female traits that affect their response to male spines are both under direct selection to minimize harm but are also under indirect selection (a good genes effect), consistent with the evolution of mating and fertilization biases being affected by several simultaneous processes.

The evolution of developmental thresholds and reaction norms for age and size at maturity.

Developing organisms typically mature earlier and at larger sizes in favorable growth conditions, while in rarer cases, maturity is delayed. The rarer reaction norm is easily accommodated by general life history models, whereas the common pattern is not. Theory suggests that a solution to this paradox lies in the existence of critical size thresholds at which maturation or metamorphosis can commence, and in the evolution of these threshold sizes in response to environmental variation. For example, ephemeral environments might favor the evolution of smaller thresholds, enabling earlier maturation. The threshold model makes two unique and untested predictions. First, reaction norms for age and size should steepen, and even change sign, with decreases in threshold size; second, food reductions at sizes below the threshold should delay maturation, while those occurring after the threshold should accelerate maturation. We test these predictions through food manipulations in five damselfly species that theory suggests should differ in threshold size. The results provide strong support for the threshold model's predictions. In all species, early food reductions delayed maturation, while late reductions accelerated maturation. Reaction norms were steeper, and the effect of food reductions changed from decelerating to accelerating at a much smaller size in species from ephemeral habitats. These results support the view that developmental thresholds can account for the widespread observation of negative correlations between age and size at maturity. Moreover, evolution of the threshold appears to be both predictable and central to the observed diversity of reaction norms for age and size at maturity.

Extinction and the temporal distribution of macroevolutionary bursts.

Phenotypic evolution through deep time is slower than expected from microevolutionary rates. This is the paradox of stasis. Previous models suggest stasis occurs because populations track adaptive peaks that remain relatively stable on million-year intervals, raising the equally perplexing question of why these large changes are so rare. Here, we consider the possibility that peaks can move more rapidly than populations can adapt, resulting in extinction. We model peak movement with explicit population dynamics, parameterized with published microevolutionary estimates. Allowing extinction greatly increases the parameter space of peak movements that yield the appearance of stasis observed in real data through deep time. Extreme peak displacements, regardless of their frequency, will rarely result in an equivalent degree of trait evolution because of extinction. Thus, larger peak displacements will rarely be inferred using trait data from extant species or observed in fossil records. Our work highlights population ecology as an important contributor to macroevolutionary dynamics, presenting an alternative perspective on the paradox of stasis, where apparent constraint on phenotypic evolution in deep time reflects our restricted view of the subset of earth's lineages that were fortunate enough to reside on relatively stable peaks.

Climate change has different predicted effects on the range shifts of two hybridizing ambush bug (Phymata, Family Reduviidae, Order Hemiptera) species.

AIM: A universal attribute of species is that their distributions are limited by numerous factors that may be difficult to quantify. Furthermore, climate change-induced range shifts have been reported in many taxa, and understanding the implications of these shifts remains a priority and a challenge. Here, we use Maxent to predict current suitable habitat and to project future distributions of two closely related, parapatrically distributed Phymata species in light of anthropogenic climate change. LOCATION: North America. TAXON: Phymata americana Melin 1930 and Phymata pennsylvanica Handlirsch 1897, Family: Reduviidae, Order: Hemiptera. METHODS: We used the maximum entropy modeling software Maxent to identify environmental variables maintaining the distribution of two Phymata species, Phymata americana and Phymata pennsylvanica. Species occurrence data were collected from museum databases, and environmental data were collected from WorldClim. Once we gathered distribution maps for both species, we created binary suitability maps of current distributions. To predict future distributions in 2050 and 2070, the same environmental variables were used, this time under four different representative concentration pathways: RCP2.6, RCP4.5, RCP6.0, and RCP8.5; as well, binary suitability maps of future distributions were also created. To visualize potential future hybridization, the degree of overlap between the two Phymata species was calculated. RESULTS: The strongest predictor to P. americana ranges was the mean temperature of the warmest quarter, while precipitation of the driest month and mean temperature of the warmest quarter were strong predictors of P. pennsylvanica ranges. Future ranges for P. americana are predicted to increase northwestward at higher CO2 concentrations. Suitable ranges for P. pennsylvanica are predicted to decrease with slight fluctuations around range edges. There is an increase in overlapping ranges of the two species in all future predictions. MAIN CONCLUSIONS: These evidences for different environmental requirements for P. americana and P. pennsylvanica account for their distinct ranges. Because these species are ecologically similar and can hybridize, climate change has potentially important eco-evolutionary ramifications. Overall, our results are consistent with effects of climate change that are highly variable across species, geographic regions, and over time.

Density-dependent offspring interactions do not explain macroevolutionary scaling of adult size and offspring size.

Most life forms exhibit a correlated evolution of adult size (AS) and size at independence (SI), giving rise to AS-SI scaling relationships. Theory suggests that scaling arises because relatively large adults have relatively high reproductive output, resulting in strong density-dependent competition in early life, where large size at independence provides a competitive advantage to juveniles. The primary goal of our study is to test this density hypothesis, using large datasets that span the vertebrate tree of life (fishes, amphibians, reptiles, birds, and mammals). Our secondary goal is to motivate new hypotheses for AS-SI scaling by exploring how subtle variation in life-histories among closely related species is associated with variation in scaling. Our phylogenetically informed comparisons do not support the density hypothesis. Instead, exploration of AS-SI scaling among life-history variants suggests that steeper AS-SI scaling slopes are associated with evolutionary increases in size at independence. We suggest that a positive association between size at independence and juvenile growth rate may represent an important mechanism underlying AS-SI scaling, a mechanism that has been underappreciated by theorists. If faster juvenile growth is a consequence of evolutionary increases in size at independence, this may help offset the cost of delayed maturation, leading to steeper AS-SI scaling slopes.

The contribution of sexual selection to ecological and mutation-order speciation.

Abundant evidence supports a role for sexual selection in the evolution of reproductive isolation, and it is thus unsurprising that much attention has been given, both conceptually and empirically, to understanding its role in speciation. In doing so, debate has arisen on how sexual selection fits within the much used ecological versus mutation-order classification of speciation mechanisms, with sexual selection often presented as a distinct third alternative. We argue that models of speciation by sexual selection include a fundamental role of divergent selection between environments or mutation order in initiating the process. Rather than representing a unique mechanism, sexual selection layers a coevolutionary process between males and females on top of the classic mechanisms such that the evolution of each sex can now be driven by divergent selection, mutation order, and selection arising from interactions with the other sex. In addition to blurring the distinction between ecological and mutation-order speciation, this coevolutionary process is likely to speed divergence. Sexual selection is not unique in this way; coevolutionary processes can similarly arise from ecological interactions between populations or species, with similar results. Ultimately, understanding the contribution of sexual selection to speciation will require identifying the processes that drive the divergence of mating biases.