Thomas E. Reimchen

Human predators outpace other agents of trait change in the wild

The observable traits of wild populations are continually shaped and reshaped by the environment and numerous agents of natural selection, including predators. In stark contrast with most predators, humans now typically exploit high proportions of prey populations and target large, reproductive-aged adults. Consequently, organisms subject to consistent and strong ‘harvest selection’ by fishers, hunters, and plant harvesters may be expected to show particularly rapid and dramatic changes in phenotype. However, a comparison of the rate at which phenotypic changes in exploited taxa occurs relative to other systems has never been undertaken. Here, we show that average phenotypic changes in 40 human-harvested systems are much more rapid than changes reported in studies examining not only natural (n = 20 systems) but also other human-driven (n = 25 systems) perturbations in the wild, outpacing them by >300% and 50%, respectively. Accordingly, harvested organisms show some of the most abrupt trait changes ever observed in wild populations, providing a new appreciation for how fast phenotypes are capable of changing. These changes, which include average declines of almost 20% in size-related traits and shifts in life history traits of nearly 25%, are most rapid in commercially exploited systems and, thus, have profound conservation and economic implications. Specifically, the widespread potential for transitively rapid and large effects on size- or life history-mediated ecological dynamics might imperil populations, industries, and ecosystems.

GLOBAL SURVEY OF MITOCHONDRIAL DNA SEQUENCES IN THE THREESPINE STICKLEBACK: EVIDENCE FOR RECENT MIGRATIONS

Phylogenetic analyses of mitochondrial DNA (mtDNA) sequences were used to assess the matriarchal genetic structure of the threespine stickleback, Gasterosteus aculeatus. A 747 base‐pair (bp) fragment of the cytochrome b was sequenced from 36 individuals collected from 25 localities in Europe, North America, and Japan. Two major divergent clades were revealed: one widespread in Japan but with representatives in some Alaskan and British Columbian lakes and the other common in Europe and North America. A simple diagnostic test using the polymerase chain reaction (PCR) and a restriction enzyme was used to assay additional individuals, confirming the absence of the Japanese clade in the Atlantic basin. Geographic distribution of mtDNA variation suggests (1) a recent origin of the Atlantic populations, and (2) support for previous hypotheses about the existence of Pleistocene refugia for freshwater fishes in Alaska and British Columbia. Silent substitution rates were used to date the colonization of the Atlantic at 90,000 to 260,000 yr before present, which conflicts with earlier dates implied by the fossil record. The recent replacement of Atlantic mitochondrial lineages suggested by our data may be explained by severe reduction or extinction of northern Atlantic populations during the Pleistocene, followed by a recent reinvasion from the Pacific. With a global perspective of the distribution of genetic variation as a framework, meaningful comparisons at a smaller geographical scale will now be possible.

A genome-wide SNP genotyping array reveals patterns of global and repeated species-pair divergence in sticklebacks

Genes underlying repeated adaptive evolution in natural populations are still largely unknown. Stickleback fish (Gasterosteus aculeatus) have undergone a recent dramatic evolutionary radiation, generating numerous examples of marine-freshwater species pairs and a small number of benthic-limnetic species pairs found within single lakes [1]. We have developed a new genome-wide SNP genotyping array to study patterns of genetic variation in sticklebacks over a wide geographic range, and to scan the genome for regions that contribute to repeated evolution of marine-freshwater or benthic-limnetic species pairs. Surveying 34 global populations with 1,159 informative markers revealed substantial genetic variation, with predominant patterns reflecting demographic history and geographic structure. After correcting for geographic structure and filtering for neutral markers, we detected large repeated shifts in allele frequency at some loci, identifying both known and novel loci likely contributing to marine-freshwater and benthic-limnetic divergence. Several novel loci fall close to genes implicated in epithelial barrier or immune functions, which have likely changed as sticklebacks adapt to contrasting environments. Specific alleles differentiating sympatric benthic-limnetic species pairs are shared in nearby solitary populations, suggesting an allopatric origin for adaptive variants and selection pressures unrelated to sympatry in the initial formation of these classic vertebrate species pairs.

Population genomics of parallel phenotypic evolution in stickleback across stream–lake ecological transitions

Understanding the genetics of adaptation is a central focus in evolutionary biology. Here, we use a population genomics approach to examine striking parallel morphological divergences of parapatric stream–lake ecotypes of threespine stickleback fish in three watersheds on the Haida Gwaii archipelago, western Canada. Genome-wide variation at greater than 1000 single nucleotide polymorphism loci indicate separate origin of giant lake and small-bodied stream fish within each watershed (mean FST between watersheds = 0.244 and within = 0.114). Genome scans within watersheds identified a total of 21 genomic regions that are highly differentiated between ecotypes and are probably subject to directional selection. Most outliers were watershed-specific, but genomic regions undergoing parallel genetic changes in multiple watersheds were also identified. Interestingly, several of the stream–lake outlier regions match those previously identified in marine–freshwater and benthic–limnetic genome scans, indicating reuse of the same genetic loci in different adaptive scenarios. We also identified multiple new outlier loci, which may contribute to unique aspects of differentiation in stream–lake environments. Overall, our data emphasize the important role of ecological boundaries in driving both local and broadly occurring parallel genetic changes during adaptation.

Landscape heterogeneity and marine subsidy generate extensive intrapopulation niche diversity in a large terrestrial vertebrate

1. Inquiries into niche variation within populations typically focus on proximate ecological causes such as competition. Here we examine how landscape heterogeneity and allochthonous (marine) subsidy might ultimately generate intrapopulation niche diversity. 2. Using stable isotope analysis, we detected extensive terrestrial-marine isotopic niche variation among subpopulations, social groups, and individual grey wolves (Canis lupus) that occupy a spatially heterogeneous landscape in coastal British Columbia comprising a mainland area and adjacent archipelago. 3. The inner island subpopulation exhibited the widest isotopic niche in the population, consuming extensive terrestrial and marine resources. Mainland and outer island subpopulations occupied comparatively narrow and primarily terrestrial, and primarily marine, niches respectively. Within these biogeographical subpopulations, social groups also diverged in niche. 4. To support examination at the individual level, we used an isotopic approach to test Van Valens (1965) niche variation hypothesis. Consistent with the hypothesis, we observed that among-individual variation increased with subpopulation niche width. 5. Patterns at all levels related to how a spatially heterogeneous coastal landscape structured the competitive environment, which in turn mediated the availability and use of terrestrial and marine resources. Broadly, our results suggest that spatial heterogeneity and allochthonous subsidy--both widespread but commonly subject to contemporary anthropogenic change--might provide novel opportunities for examination and conservation of ecological variation within populations.

PREDATOR HANDLING FAILURES OF LATERAL PLATE MORPHS IN GASTEROSTEUS ACULEATUS: FUNCTIONAL IMPLICATIONS FOR THE ANCESTRAL PLATE CONDITION

Summary The completely plated morph in the threespine stickleback ( Gasterosteus aculeatus ) is considered to be the ancestral plate condition and is the predominant morph inhabiting marine waters and numerous northern freshwaters. Evolutionary aspects of this distribution have been widely addressed yet functional mechanisms remain obscure. Experiments described here using the common piscivore ( Oncorhynchus clarki ) show that the posterior plates of G. aculeatus interfere with the swallowing abilities of the piscivore, possibly by disrupting pharyngeal jaw retraction, and this leads to increased escape opportunities of the stickleback. The advantage of the completely plated condition is most expressed at higher ratios of prey diameter to predator mouth diameter and appears to havea defensive effect comparable to that of dorsal and pelvic spines. This attribute, combined with the physical protection that plates offer against puncturing, would be particularly benee cial where there is high probability of capture by toothed predators. Such a selection regime appears to characterize the predominantly limnetic and pelagic habitats where marine stickleback are found and may account for the wide geographical distribution of the completely plated morph and its persistence from the Miocene.

TEMPORAL VARIATION IN DIVERGENT SELECTION ON SPINE NUMBER IN THREESPINE STICKLEBACK

Abstract.— Short‐term temporal cycles in ecological pressures, such as shifts in predation regime, are widespread in nature yet estimates of temporal variation in the direction and intensity of natural selection are few. Previous work on threespine stickleback (Gasterosteus aculeatus) has revealed that dorsal and pelvic spines are a defense against gape‐limited predators but may be detrimental against grappling insect predators. In this study, we examined a 15‐year database from an endemic population of threespine stickleback to look for evidence of temporal shifts in exposure to these divergent predation regimes and correlated shifts in selection on spine number. For juveniles, we detected selection for increased spine number during winter when gape‐limited avian piscivores were most common but selection for decreased spine number during summer when odonate predation was more common. For subadults and adults, which are taken primarily by avian piscivores, we predicted selection should generally be for increased spine number in all seasons. Among 59 comparisons, four selection differentials were significant (Bonferroni corrected) and in the predicted direction. However, there was also substantial variability in remaining differentials, including two examples with strong selection for spine reduction. These reversals were associated with increased tendency of the fish to shift to a benthic niche, as determined from examination of stomach contents. These dietary data suggest that increased encounter rates with odonate predation select for spine reduction. Strong selection on spine number was followed by changes in mean spine number during subsequent years and a standard quantitative genetic formula revealed that spine number has a heritable component. Our results provide evidence of rapid morphological responses to selection from predators and suggest that temporal variation in selection may help maintain variation within populations. Furthermore, our findings indicate that variable selection can be predicted if the agents of selection are known.

The unique ecology of human predators

An anomalous and unbalanced predator In the past century, humans have become the dominant predator across many systems. The species that we target are thus far in considerable decline; however, predators in the wild generally achieve a balance with their prey populations such that both persist. Darimont et al. found several specific differences between how humans and other predatory species target prey populations (see the Perspective by Worm). In marine environments, for example, we regularly prey on other predator species. These differences may contribute to our much larger ecological impact when compared with other predators. Science, this issue p. 858; see also p. 784 Human predators do not mimic the behavior of natural predators. [Also see Perspective by Worm] Paradigms of sustainable exploitation focus on population dynamics of prey and yields to humanity but ignore the behavior of humans as predators. We compared patterns of predation by contemporary hunters and fishers with those of other predators that compete over shared prey (terrestrial mammals and marine fishes). Our global survey (2125 estimates of annual finite exploitation rate) revealed that humans kill adult prey, the reproductive capital of populations, at much higher median rates than other predators (up to 14 times higher), with particularly intense exploitation of terrestrial carnivores and fishes. Given this competitive dominance, impacts on predators, and other unique predatory behavior, we suggest that humans function as an unsustainable “super predator,” which—unless additionally constrained by managers—will continue to alter ecological and evolutionary processes globally.

VARIABLE PREDATION REGIMES PREDICT THE EVOLUTION OF SEXUAL DIMORPHISM IN A POPULATION OF THREESPINE STICKLEBACK

Abstract Sexual dimorphism is widespread in nature and can be influenced by sex‐specific natural selection resulting from ecological differences between the sexes. Here we show that contrasting life‐history pressures and temporal shifts in ecology can exert a strong influence on the evolution of sexual dimorphism. The bony spines exhibited by stickleback are a defense against open‐water avian predators but may be detrimental against benthic macroinvertebrate predators. Female stickleback from a coastal lake in western Canada occupy a more open‐water ecological niche and exhibit greater dorsal and pelvic spine number than males, but the magnitude of these differences varies among life‐history stages, seasons, and years. Ecological data on diet and parasite load and 62 seasonal estimates of selection over a 15‐year period show that selection favors increased spine number in females and decreased spine number in males, but only when pronounced ecological differences between the sexes results in differential exposure to the two, divergent predation regimes. Thus occasional sex‐reversals in ecological niche reversed the mode of selection. These processes caused a predictable response in the subsequent generation, indicating that divergent predation caused evolutionary change in dimorphism. However, temporal oscillations in sex‐specific selection resulted in no net change in sexual dimorphism over the 15‐year study period, indicating that fluctuations in directional selection can be responsible for long‐term stasis. Replicated shifts in selective regime can demonstrate the primacy of ecological processes in driving evolution and our results illustrate how such shifts are detectable using long‐term monitoring of natural populations.

Predator-Induced Cyclical Changes in Lateral Plate Frequencies of Gasterosteus

This study investigates ecological aspects to intrapopulation variability in the lateral plates of threespine stickleback (Gasterosteus aculeatus) at a coastal lake in western Canada. The frequency distribution of the plates, which was slightly skewed to the right and leptokurtic, varied spatially and seasonally. Cyclical frequency changes in plates were most pronounced on sub-adult size classes and these closely tracked (multiple r = 0.77) seasonal differences in the relative proportion of the two major predator groups, trout and diving birds. Trout predation was correlated with an increase in plate number while bird predation was correlated with a reduction in plate number. Such divergent selection pressures, which are probably common in natural populations, would account for the presence of multiple phenotypes and allow for rapid shifts in defensive morphology among different populations where predation regime differs.