Kiyoko M. Gotanda

The spatial patterns of directional phenotypic selection.

Local adaptation, adaptive population divergence and speciation are often expected to result from populations evolving in response to spatial variation in selection. Yet, we lack a comprehensive understanding of the major features that characterise the spatial patterns of selection, namely the extent of variation among populations in the strength and direction of selection. Here, we analyse a data set of spatially replicated studies of directional phenotypic selection from natural populations. The data set includes 60 studies, consisting of 3937 estimates of selection across an average of five populations. We performed meta-analyses to explore features characterising spatial variation in directional selection. We found that selection tends to vary mainly in strength and less in direction among populations. Although differences in the direction of selection occur among populations they do so where selection is often weakest, which may limit the potential for ongoing adaptive population divergence. Overall, we also found that spatial variation in selection appears comparable to temporal (annual) variation in selection within populations; however, several deficiencies in available data currently complicate this comparison. We discuss future research needs to further advance our understanding of spatial variation in selection.

Body size and reserve protection affect flight initiation distance in parrotfishes

Flight initiation distance (FID), the distance at which an organism begins to flee an approaching threat, is an important component of antipredator behavior and a potential indicator of an animal’s perception of threat. In a field study on parrotfishes, we tested the predictions that FID in response to a diver will increase with body size, a correlate of reproductive value, and with experience of threat from humans. We studied a broad size range in four species on fringing reefs inside and outside the Barbados Marine Reserve. We used the Akaikes Information Criterion modified for small sample sizes (AICc) and model averaging to select and assess alternative models. Body size, reserve protection, and distance to a refuge, but not species, had strong support in explaining FID. FID increased with body size and generally remained two to ten times fish total length. FID was greater outside the reserve, especially in larger fish. Although we were not able to completely rule out other effects of size or reserve, this study supports predictions of an increase in FID with reproductive value and threat from humans.

Precipitation drives global variation in natural selection

Climate-driven selection Climate change will fundamentally alter many aspects of the natural world. To understand how species may adapt to this change, we must understand which aspects of the changing climate exert the most powerful selective forces. Siepielski et al. looked at studies of selection across species and regions and found that, across biomes, the strongest sources of selection were precipitation and transpiration changes. Importantly, local and regional climate change explained patterns of selection much more than did global change. Science, this issue p. 959 Local and regional climate changes in rainfall explain patterns of species selection across biomes more than global change. Climate change has the potential to affect the ecology and evolution of every species on Earth. Although the ecological consequences of climate change are increasingly well documented, the effects of climate on the key evolutionary process driving adaptation—natural selection—are largely unknown. We report that aspects of precipitation and potential evapotranspiration, along with the North Atlantic Oscillation, predicted variation in selection across plant and animal populations throughout many terrestrial biomes, whereas temperature explained little variation. By showing that selection was influenced by climate variation, our results indicate that climate change may cause widespread alterations in selection regimes, potentially shifting evolutionary trajectories at a global scale.

Human influences on evolution, and the ecological and societal consequences

Humans have dramatic, diverse and far-reaching influences on the evolution of other organisms. Numerous examples of this human-induced contemporary evolution have been reported in a number of ‘contexts’, including hunting, harvesting, fishing, agriculture, medicine, climate change, pollution, eutrophication, urbanization, habitat fragmentation, biological invasions and emerging/disappearing diseases. Although numerous papers, journal special issues and books have addressed each of these contexts individually, the time has come to consider them together and thereby seek important similarities and differences. The goal of this special issue, and this introductory paper, is to promote and expand this nascent integration. We first develop predictions as to which human contexts might cause the strongest and most consistent directional selection, the greatest changes in evolutionary potential, the greatest genetic (as opposed to plastic) changes and the greatest effects on evolutionary diversification. We then develop predictions as to the contexts where human-induced evolutionary changes might have the strongest effects on the population dynamics of the focal evolving species, the structure of their communities, the functions of their ecosystems and the benefits and costs for human societies. These qualitative predictions are intended as a rallying point for broader and more detailed future discussions of how human influences shape evolution, and how that evolution then influences species traits, biodiversity, ecosystems and humans. This article is part of the themed issue ‘Human influences on evolution, and the ecological and societal consequences’.

Adding parasites to the guppy-predation story: insights from field surveys

Studies of phenotypic variation in nature often consider only a single potential selective agent. In such cases, it remains an open question as to whether variation attributed to that single measured agent might be influenced by some other unmeasured agent. Previous research has shown that phenotypic variation in the Trinidadian guppy (Poecilia reticulata) is strongly influenced by predation regime, and we here ask whether parasitism might represent an additional important selective agent shaping this variation. We performed a field survey of 26 natural guppy populations of known predation regime in northern Trinidad. We quantified levels of parasitism of guppies by the monogenean ecotoparasite, Gyrodactylus, and examined whether this parasite was associated with guppy body size or male colour. Spatial variation in Gyrodactylus parasitism was consistent between years, and parasite prevalence was generally, but not always, higher at high-predation sites than at low-predation sites. Consistent with previous work, predation regime was related to guppy size and some aspects of male colour, whereas parasitism showed few and only minor associations with the same traits. Moreover, a consideration of parasitism did not alter any interpretations regarding associations between guppy traits and predation regimes. These results suggest that parasitism, at least as quantified in the present study, does not play a major role in shaping variation in guppy body size or colour. Nevertheless, considerable variation in these traits, even within a predation regime, suggests the likely importance of other selective agents beyond just predation regime.

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.

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.

Galapagos Mockingbird (Mimus parvulus) Preys on an Invasive Mammal

ABSTRACT Galapagos Mockingbirds (Mimus parvulus) are opportunistic feeders that have been observed engaging in a variety of unusual predatory behaviors. Here, we report on a specific behavior that we observed: a Galapagos Mockingbird preying on an invasive mammal by repeatedly hitting it on the ground. We discuss the reasons that the mockingbird might have engaged in this behavior and the potential implications this could have for native biodiversity and conservation on the Galapagos Islands.

Response to Comment on “Precipitation drives global variation in natural selection”

The comment by Myers-Smith and Myers focuses on three main points: (i) the lack of a mechanistic explanation for climate-selection relationships, (ii) the appropriateness of the climate data used in our analysis, and (iii) our focus on estimating climate-selection relationships across (rather than within) taxonomic groups. We address these critiques in our response.

Urbanization erodes niche segregation in Darwin's finches

Urbanization is influencing patterns of biological evolution in ways that are only beginning to be explored. One potential effect of urbanization is in modifying ecological resource distributions that underlie niche differences and that thus promote and maintain species diversification. Few studies have assessed such modifications, or their potential evolutionary consequences, in the context of ongoing adaptive radiation. We study this effect in Darwins finches on the Galápagos Islands, by quantifying feeding preferences and diet niche partitioning across sites with different degrees of urbanization. We found higher finch density in urban sites and that feeding preferences and diets at urban sites skew heavily toward human food items. Furthermore, we show that finches at urban sites appear to be accustomed to the presence of people, compared with birds at sites with few people. In addition, we found that human behavior via the tendency to feed birds at non‐urban but tourist sites is likely an important driver of finch preferences for human foods. Site differences in diet and feeding behavior have resulted in larger niche breadth within finch species and wider niche overlap between species at the urban sites. Both factors effectively minimize niche differences that would otherwise facilitate interspecies coexistence. These findings suggest that both human behavior and ongoing urbanization in Galápagos are starting to erode ecological differences that promote and maintain adaptive radiation in Darwins finches. Smoothing of adaptive landscapes underlying diversification represents a potentially important yet underappreciated consequence of urbanization. Overall, our findings accentuate the fragility of the initial stages of adaptive radiation in Darwins finches and raise concerns about the fate of the Galápagos ecosystems in the face of increasing urbanization.