Gregor Rolshausen

Contemporary Evolution of Reproductive Isolation and Phenotypic Divergence in Sympatry along a Migratory Divide

Understanding the influence of human-induced changes on the evolutionary trajectories of populations is a fundamental problem [1, 2]. The evolution of reproductive isolation in sympatry is rare, relying on strong selection along steep ecological gradients [3-7]. Improved wintering conditions owing to human activities promoted the recent establishment of a migratory divide in Central European blackcaps (Sylvia atricapilla) [8, 9]. Here, we show that differential migratory orientation facilitated reproductive isolation of sympatric populations within <30 generations. The genetic divergence in sympatry exceeds that of allopatric blackcaps separated by 800 km and is associated with diverse phenotypic divergence. Blackcaps migrating along the shorter northwestern route have rounder wings and narrower beaks and differ in beak and plumage color from sympatric southwest-migrating birds. We suggest that distinct wing and beak morphologies are ecomorphological adaptations resulting from divergent, multifarious selection regimes during migration. We hypothesize that restricted gene flow accelerates the evolution of adaptive phenotypic divergence toward the contrasting selection regimes. Similar adaptive processes can occur in more than 50 bird species that recently changed their migratory behavior [10, 11] or in species with low migratory connectivity. Our study thus illustrates how ecological changes can rapidly drive the contemporary evolution of ecotypes.

Aphids do not attend to leaf colour as visual signal, but to the handicap of reproductive investment

Abstract The evolution of visual warning signals is well known in animals but has received scant attention in plants. The coevolutionary hypothesis is the most influential hypothesis on warning signals in plants proposing that red and yellow leaf colours in autumn signal defensive strength to herbivores. So far, evidence in support of the hypothesis, which assumes a coevolutionary origin of autumnal leaf colours, is correlative and open to alternative explanations. We therefore tested the coevolutionary hypothesis experimentally by colouring the leaves either red or green of same-aged mountain ash (Sorbus aucuparia) individuals. We monitored the response of winged aphids to leaf colour using insect glue on branches with natural and artificial leaf colours in each individual. In contrast to the prediction of the coevolutionary hypothesis, aphid numbers did not differ between the individuals with artificial green or artificial red leaves. Likewise, at the within-plant level, aphids did not colonize branches with natural green leaves preferentially. However, we suggest that plants emitted warning signals because aphids colonized the hosts non-randomly. We found a strong positive correlation between aphid numbers and fruit production, suggesting an allocation trade-off between investment in plant defence and reproduction. Our study demonstrates that aphids use warning signals or cues in host selection, probably volatiles, but that they did not use leaf colour.

Contrasting Patterns of Genetic Differentiation among Blackcaps (Sylvia atricapilla) with Divergent Migratory Orientations in Europe

Migratory divides are thought to facilitate behavioral, ecological, and genetic divergence among populations with different migratory routes. However, it is currently contentious how much genetic divergence is needed to maintain distinct migratory behavior across migratory divides. Here we investigate patterns of neutral genetic differentiation among Blackcap (Sylvia atricapilla) populations with different migratory strategies across Europe. We compare the level of genetic divergence of populations migrating to southwestern (SW) or southeastern (SE) wintering areas with birds wintering in the British Isles following a recently established northwesterly (NW) migration route. The migratory divide between SW and SE wintering areas can be interpreted as a result of a re-colonization process after the last glaciation. Thus we predicted greater levels of genetic differentiation among the SW/SE populations. However, a lack of genetic differentiation was found between SW and SE populations, suggesting that interbreeding likely occurs among Blackcaps with different migratory orientations across a large area; therefore the SW/SE migratory divide can be seen as diffuse, broad band and is, at best, a weak isolating barrier. Conversely, weak, albeit significant genetic differentiation was evident between NW and SW migrants breeding sympatrically in southern Germany, suggesting a stronger isolating mechanism may be acting in this population. Populations located within/near the SW/SE contact zone were the least genetically divergent from NW migrants, confirming NW migrants likely originated from within the contact zone. Significant isolation-by-distance was found among eastern Blackcap populations (i.e. SE migrants), but not among western populations (i.e. NW and SW migrants), revealing different patterns of genetic divergence among Blackcap populations in Europe. We discuss possible explanations for the genetic structure of European Blackcaps and how gene flow influences the persistence of divergent migratory behaviors.

Does plasticity enhance or dampen phenotypic parallelism? A test with three lake-stream stickleback pairs.

Parallel (and convergent) phenotypic variation is most often studied in the wild, where it is difficult to disentangle genetic vs. environmentally induced effects. As a result, the potential contributions of phenotypic plasticity to parallelism (and nonparallelism) are rarely evaluated in a formal sense. Phenotypic parallelism could be enhanced by plasticity that causes stronger parallelism across populations in the wild than would be expected from genetic differences alone. Phenotypic parallelism could be dampened if site‐specific plasticity induced differences between otherwise genetically parallel populations. We used a common‐garden study of three independent lake–stream stickleback population pairs to evaluate the extent to which adaptive divergence has a genetic or plastic basis, and to investigate the enhancing vs. dampening effects of plasticity on phenotypic parallelism. We found that lake–stream differences in most traits had a genetic basis, but that several traits also showed contributions from plasticity. Moreover, plasticity was much more prevalent in one watershed than in the other two. In most cases, plasticity enhanced phenotypic parallelism, whereas in a few cases, plasticity had a dampening effect. Genetic and plastic contributions to divergence seem to play a complimentary, likely adaptive, role in phenotypic parallelism of lake–stream stickleback. These findings highlight the value of formally comparing wild‐caught and laboratory‐reared individuals in the study of phenotypic parallelism.

Do aphids paint the tree red (or yellow) - can herbivore resistance or photoprotection explain colourful leaves in autumn?

We explored two mutually nonexclusive hypotheses on autumnal leaf colouration. The co-evolutionary hypothesis states that autumnal leaf colouration functions as a handicap signal to herbivorous insects, whereas the photoprotection hypothesis posits that plant pigments primarily protect the plant against cold-induced photoinhibition and enhance nutrient transfer. To contrast both hypotheses, we compared yellow and red leaf colouration in three groups of mountain ash (Sorbus aucuparia L.). Two montane groups of different age were characterised by low aphid numbers and low temperature, and a lowland group by high aphid numbers and high temperature. There were no consistent altitudinal differences in leaf colouration. Compared to young trees, adult trees developed fewer red but more yellow leaves at high altitude. In the lowland population, the development of red leaf colour was related to decreasing daytime temperature, whereas the appearance of yellow leaf colouration corresponded to the decreasing photoperiod. This is consistent with the photoprotection hypothesis. Individual differences in red and yellow leaf colouration were inversely correlated to the number of fruits, which might be interpreted as a trade-off between reproductive and protective commitment.Temperature effects explained variation in aphid numbers over time and leaf colouration explained aphid distribution on a given day. As predicted by the co-evolutionary hypothesis, strongly coloured individuals harboured fewer aphids than green or dull-coloured ones. Since decreasing temperature reduced the number of migrating aphids but induced red leaf colouration, these processes are not mutually fine-tuned, which likely restricts the potential for co-evolution between mountain ash and aphids.

How Parallel Is Parallel Evolution? A Comparative Analysis in Fishes

Evidence of phenotypic parallelism is often used to infer the deterministic role played by natural selection. However, variation in the extent or direction of divergence is often evident among independent evolutionary replicates, raising the following question: just how parallel, overall, is parallel evolution? We answer this question through a comparative analysis of studies of fishes, a taxon where parallel evolution has been much discussed. We first ask how much of the among-population variance in phenotypic traits can be explained by different “environment” types, such as high predation versus low predation or benthic versus limnetic. We then use phenotypic change vector analysis to quantify variation in the direction (vector angles) and magnitude (vector lengths) of environment-associated divergence. All analyses show high variation in the extent of parallelism—from very high to very low, along with everything in between—highlighting the importance of quantifying parallelism rather than just asserting its presence. Interestingly, instances of low extents of parallelism represent important components of divergence in many cases, promising considerable opportunities for inferences about the factors shaping phenotypic divergence.

Do stressful conditions make adaptation difficult? Guppies in the oil-polluted environments of southern Trinidad.

The ability of populations to rapidly adapt to new environments will determine their future in an increasingly human‐modified world. Although meta‐analyses do frequently uncover signatures of local adaptation, they also reveal many exceptions. We suggest that particular constraints on local adaptation might arise when organisms are exposed to novel stressors, such as anthropogenic pollution. To inform this possibility, we studied the extent to which guppies (Poecilia reticulata) show local adaptation to oil pollution in southern Trinidad. Neutral genetic markers revealed that paired populations in oil‐polluted versus not‐polluted habitats diverged independently in two different watersheds. Morphometrics revealed some divergence (particularly in head shape) between these environments, some of which was parallel between rivers. Reciprocal transplant experiments in nature, however, found little evidence of local adaptation based on survival and growth. Moreover, subsequent laboratory experiments showed that the two populations from oil‐polluted sites showed only weak local adaptation even when compared to guppies from oil‐free northern Trinidad. We conclude that guppies show little local adaptation to oil pollution, which might result from the challenges associated with adaptation to particularly stressful environments. It might also reflect genetic drift owing to small population sizes and/or high gene flow between environments.

Linking macrotrends and microrates: Re-evaluating microevolutionary support for Cope's rule

Copes rule, wherein a lineage increases in body size through time, was originally motivated by macroevolutionary patterns observed in the fossil record. More recently, some authors have argued that evidence exists for generally positive selection on individual body size in contemporary populations, providing a microevolutionary mechanism for Copes rule. If larger body size confers individual fitness advantages as the selection estimates suggest, thereby explaining Copes rule, then body size should increase over microevolutionary time scales. We test this corollary by assembling a large database of studies reporting changes in phenotypic body size through time in contemporary populations, as well as studies reporting average breeding values for body size through time. Trends in body size were quite variable with an absence of any general trend, and many populations trended toward smaller body sizes. Although selection estimates can be interpreted to support Copes rule, our results suggest that actual rates of phenotypic change for body size cannot. We discuss potential reasons for this discrepancy and its implications for the understanding of Copes rule.

Individual differences in migratory behavior shape population genetic structure and microhabitat choice in sympatric blackcaps (Sylvia atricapilla)

In migratory birds, traits such as orientation and distance are known to have a strong genetic background, and they often exhibit considerable within-population variation. How this variation relates to evolutionary responses to ongoing selection is unknown because the underlying mechanisms that translate environmental changes into population genetic changes are unclear. We show that within-population genetic structure in southern German blackcaps (Sylvia atricapilla) is related to individual differences in migratory behavior. Our 3-year study revealed a positive correlation between individual migratory origins, denoted via isotope (δ2H) values, and genetic distances. Genetic diversity and admixture differed not only across a recently established migratory polymorphism with NW- and SW-migrating birds but also across δ2H clusters within the same migratory route. Our results suggest assortment based on individual migratory origins which would facilitate evolutionary responses. We scrutinized arrival times and microhabitat choice as potential mechanisms mediating between individual variation in migratory behavior and assortment. We found significant support that microhabitat choice, rather than timing of arrival, is associated with individual variation in migratory origins. Moreover, examining genetic diversity across the migratory divide, we found migrants following the NW route to be genetically more distinct from each other compared with migrants following the traditional SW route. Our study suggests that migratory behavior shapes population genetic structure in blackcaps not only across the migratory divide but also on an individual level independent of the divide. Thus, within-population variation in migratory behavior might play an important role in translating environmental change into genetic change.

Magic traits: distinguishing the important from the trivial

Servedio et al. [1], following Gavrilets [2], define a magictrait as ‘a trait subject to divergent selection and a traitcontributing to non-random mating that are pleiotropicexpressions of the same gene(s)’. This clarified definition iscertainly helpful, but we outline here several pivotal ques-tions for empirical research, particularly surrounding thecrucial concept of effect size.The effect size of a magic trait, defined by Servedio et al.[1] as ‘how much the trait contributed to the evolution ofincreased reproductive isolation’, determines whether amagic trait is actually important for speciation (an ‘impor-tant magic trait’)or isa ‘trivial magic trait’ (a magic trait ofvery small or zero effect size). Effect size is therefore whatmattersempirically,and yet it isabsent from thedefinitionof a magic trait, which instead embodies theoretical pre-occupations with the genetics underlying traits. We do notpropose to redefine ‘magic trait’, but instead hope to illus-trate how empirical advances will require an explicit focuson effect size. Problematically, however, the definition ofeffect size is retrospective and not generally measurable;empiricalproxiesforeffectsizethatcanbeusedpredictivelyare therefore needed. We here treat the strengths of diver-gentselection, assortativematingand pleiotropy (thethreecomponents of the magic trait definition) as the a prioriexpected contributors to effect size during speciation.Divergent (including disruptive) selection, the first pil-lar of the magic trait definition, is certainly important forspeciation;however,itsmagnitudeismoreimportantthanits mere presence [3]. Moreover, distinguishing weaklydivergent selection from the absence of selection is empiri-cally difficult [4], making it hard to determine whether atrait is magic or non-magic. Fortunately, this distinction isprobablynotofkeyimportancetotheprocessofspeciation,because magic traits under such weak selection are proba-bly trivial. The empirical focus should be on magic traitsexpected to be of large effect size.In addition, spatial and temporal variation in selection[5] makes it difficult to determine whether a trait is gener-allyunderdivergentselection.Forexample,beaksizeintheMedium Ground Finch (Geospiza fortis) has been proposedto be magic [1,6], but selection on beak size is, at varioustimes and places,directional,stabilizing, ordivergent [7,8].Consequently, it is hard to say whether beak size wouldsatisfy the definition; as the selective regime changes, beaksizeswitchesfrommagictonon-magicandbackagain.Thisimpliesthatsuchatraitis,inasense,anordinarytraitthatcontributestonon-randommating,butthatis,attimes,ina‘magic environment’ that subjects it to divergent selection;the magic comes from the trait–environment interaction.Thus, a crucial question emerges: how consistently diver-gent,throughtimeandacrossspace,mustselectionbeforatrait to be magic and also important for speciation? Again,we argue that expected effect size is the key: divergentselection must be sufficiently strong and consistent toactu-ally drive divergence.The second pillar of the definition is non-random mat-ing. However, it is also difficult to distinguish weakly non-randommating fromrandom mating(e.g. [9]), aswell astodetermine the specific trait underlying non-random mat-ing [1]. Moreover, just as with divergent selection, non-randommatingcanvaryinspaceandtime[10].Thus,allofthe difficulties raised above concerning divergent selectionapply with equal strength to non-random mating.The arch connecting these two definitional pillars ispleiotropy; if, instead, the two pillars are influenced by atightly linked pair of genes, that locus is considered only amagic trait ‘mimic’ [1]. Again, empirically differentiatingbetween these two cases is quite difficult [11]. Further-more, the distinction might be of little consequence to thedynamics of speciation; a mimic might have an effect sizejust as large as, or larger than, that of a magic trait [3].Instead, what probably matters is the strength of pleiotro-py or linkage.In summary, empirically distinguishing trivial magictraits from non-magic traits, and magic traits from mimictraits, will prove very difficult. Fortunately, these distinc-tions are largely irrelevant to many questions surroundingspeciation in nature. Instead, the important (although lessprecise) distinction is between traits expected to be of largeeffectsize(whethermagicormimic)versusthoseexpectedtobe of small effect size (whether trivial or non-magic). Tobridge the gap between theoretical and empirical perspec-tives on magic traits, we suggest an increased focus onprobableproxiesforultimateeffectsize,ontheenvironmen-talandecologicalfactorsthatarelikelytobecontributingtoeffect size, and on the evolutionary forces expected to altereffect size through time. With these priorities, a betterunderstanding of the magic of speciation can be expected.