Stickleback Research

at Clark University

Research

Table of Contents

I. Adaptive Radiation of the Threespine Stickleback

II. Geographic Variation:

Reproductive Variation and Coloration

Antipredator Traits

Life History

Parasite Effects on Phenotype: Schistocephalus solidus

III. Ancestral Phenotypic Plasticity and Evolution:

Reproductive Behavior and Coloration

Morphology

IV. Contemporary Evolution:

Life History and Morphology

Conservation

V. Global Environmental Change: Impacts on Stickleback
and their Watersheds

Adaptive Radiation of the Threespine Stickleback

Threespine stickleback (Gasterosteus aculeatus) comprises a complex of differentiated populations, many of which are clearly adapted to local environments.  This complex of freshwater populations is thus called an adaptive radiation.  The radiation is unusual in several respects.  First, the freshwater populations (peripheral images in the wheel) are thought to have evolved from a relatively uniform oceanic ancestor like that which exists in the north temperate Atlantic and Pacific oceans today (central image in the wheel).  Thus the characteristics of oceanic fish can be used to identify ancestral characteristics relative to the freshwater radiation, which is unusual in that much of this radiation has arisen since the last glacial maximum.  Between 15,000 and 20,000 yr ago ice began to retreat, permitting colonization of freshwater habitats by oceanic fish.  These populations have adapted rapidly to new habitats, often giving rise repeatedly and independently, to similar phenotypes (ecotypes) in similar environments, and sometimes, to new species.  Differences have evolved in behavior, life history and morphology.  We take advantage of this radiation to study evolution of these phenotypes by comparing freshwater ecotypes with their oceanic ancestors and by contrasting independently evolved populations within ecotypes.  These comparisons enable us to address the issues outlined below.

top

Reproductive Variation and Coloration

In northwestern North America, stickleback in small, shallow lakes have evolved a deep-bodied (benthic) form specialized for feeding on benthic invertebrates, while those in deep, oligotrophic lakes evolved a slender form (limnetic) adapted for feeding on plankton. Research in our laboratory has demonstrated that benthic populations retain ancestral tendencies to form bottom-feeding foraging groups that cannibalize young in nests when they are discovered. Courtship in benthic populations is typically initiated by females who swim to the male and press their abdomens against the male’s dorsal spines initiating the relatively inconspicuous dorsal pricking behavior that makes up most courtship in these populations. In contrast, limnetics have lost ancestral cannibalistic tendencies, and males initiate courtship with the very conspicuous zig-zag dance.

Ongoing research by Stella Richard is aimed at understanding ecotypic differences in the endocrine stress responses of males confronted by these foraging groups. Benthic males tend to be drab during courtship, whereas limnetic males typically have red throats and iridescent blue-green backs. Ancestral populations in the Pacific Northwest tend to exhibit intermediate and plastic (below) phenotypes in nature. We have also shown that benthic males retain ancestral diversionary displays in response to the approach of groups, and that these displays appear to include co-opted and ritualized elements of behavior used in other contexts. Current collaborative research with Anna Greenwood and Katie Peichel is aimed at understanding the genomic bases of this remarkable behavior.

top

Antipredator Traits

Stickleback are consumed by many predators and have evolved a diversity of antipredator defenses including spines (for which the threespine stickleback is named), bony lateral plates and a host of predator-avoidance behaviors.  Because this small fish occupies a variety of habitats, the predator assemblages to which they are exposed can differ markedly.  In lakes devoid of chasing predatory fish (e.g., salmonids) stickleback often lose much or all of their pelvic armor.  We are currently exploring the effects of salmonid introduction on the subsequent evolution of the pelvic girdle in these pelvic-reduced populations.  Our research demonstrates rapid, contemporary evolution in some of these populations (Kindinger).  Stickleback not only avoid predation by being hard to swallow, but also by being hard to catch in the first place. Ongoing research in our laboratory explores relationship between native predator environment and antipredator behavior. This research explores variation in performance and laterality of the fast-start reflex (Rana), in responses of fish from different predator environments to visual stimuli provided by different kinds of predators (Wund), and in olfactory perception of predators (Golub).  The role of learning at different life history stages in generating appropriate antipredator responses is also a focus of research in the laboratory (Golub, Wund).

lexi with tern
Lexi Messler ('05) testing stickleback response to avian shadow.

Life History

We use both field and laboratory studies to investigate the evolution of life-history traits in threespine stickleback (and to a lesser extent ninespine stickleback, Pungitius pungitius; and fourspine stickleback, Apeltes quadracus).dissected female Much of this research is based on annual (1992-present) sampling of 50-70 sites in the Cook Inlet region of Alaska, USA, and on less consistent sampling of populations in southern British Columbia, Canada (specimen collection). We have documented extensive within- and among- population variation in female reproductive traits including egg size, fecundity, size at first reproduction, as well as correlations among traits such as egg and clutch size (Baker, Heins, King). These data have guided experimental research including ongoing research on the function of egg size under varying intensities of foraging competition among fry (O’Brien). The multi-year data base has also enabled us to document rapid evolutionary change within populations. We are now initiating research on apparent population differences in the patterns of senescence across populations.

top

Parasite Effects on Phenotype: Schistocephalus solidus

The tapeworm parasite (S. solidus) infects threespine stickleback and can cause demelanization of the stickleback host and change its behavior once the worm reaches a size sufficient for White fish with parasites reproduction in the definitive host (bird). Effects of this parasite vary regionally. Research in our laboratory explores the effect of the parasite on the behavior and coloration of adult hosts(Tzarougian), changes in physiology and chromatophore condition (Richard), and in collaboration with David Heins, changes in life history and effects of the parasite on population dynamics (Baker).

Reproductive Behavior and Coloration

At the onset of adaptive differentiation induced by the colonization of novel environments, patterns of ancestral plasticity can determine which phenotypes are expressed, and thus influence the course of subsequent evolution. In this way, the pattern of ancestral plasticity can determine which behavioral phenotypes are expressed in a given environment and therefore, which phenotypes have the potential to evolve in response to selection. A primary focus of our research is to understand how ancestral plasticity in male nuptial coloration, male courtship behavior, and female mating preferences of threespine stickleback would have influenced the evolution of these traits in freshwater habitats that promoted the evolution of benthic (bottom-feeding) and limnetic (plankton-feeding) lacustrine populations.

top

Morphology

Ancestral plasticity may have played an important role in guiding the repeated evolution of benthic and limnetic ecotypes. In shallow, relatively eutrophic lakes, stickleback forage for large food in the benthos and are characterized by deep bodies, large mouths, and relatively small eyes. Stickleback populations in deeper, more oligotrophic lakes spend their lives eating plankton in the water column, and have more fusiform bodies, small, upturned mouths, and relatively large eyes. As ancestral stickleback repeatedly encountered either of these two environments, developmental plasticity may have differentially shaped their morphology, initiating the evolution of parallel patterns of divergence. Currently, we are experimentally testing whether, and to what degree, threespine stickleback from these morphologically distinct ecotypes exhibit plasticity of trophic morphology when forced to feed on alternative food types. We predict that the pattern of diet-induced plasticity in the ancestral population will mirror the pattern of phenotypic divergence between the two derived ecotypes. Furthermore, we are interested in how evolution subsequently shaped patterns of plasticity in derived populations (e.g, genetic accommodation, genetic assimilation; Wund, Baker, Clancy, Golub).

Life History and Morphology

More than 20 years of annual sampling of stickleback populations in the Alaska has enabled us to detect multiple, fascinating cases of contemporary evolution. Over a 10 yr period (five generations) we have documented evolutionary decline in egg size that was among the fastest cases of contemporary evolution ever recorded, and it was coincident with other life history changes predicted by theory. The change in egg size moved the population mean from one of the two largest in the region to the bottom percent. Other populations appear to exhibit cyclic changes in life history features, or to be responding to directional selection (primarily induced by increased productivity) with different changes in life history features (Baker). We have also observed rapid re-evolution of pelvic armoring in some, but not all populations historically devoid of piscine predators, to which predatory fish have been introduced (Kindinger). We are currently working to explain causes for the variation in patterns of contemporary evolution of life history and armor traits, and to determine whether anti-predator behavior has evolved in concert with armor (Wund, Golub).

top

Conservation

Recent adaptive radiations comprise a complex of populations that can offer special insight into the processes that generate biodiversity. The loss of unique, or scientifically important members of such radiations undermines the ability to make comparisons among divergent populations, thereby devaluing the entire radiation. For this reason, it is essential to carefully plan and apply strategies that protect either entire adaptive radiations or evolutionarily significant units that capture critical variation. The protection of critical populations within the threespine stickleback post-glacial radiation is particularly difficult for two reasons. The first is simply that threespine stickleback are very abundant, and thus a great many populations have to be surveyed in order to identify the critical ones. The second reason is that anthropogenic change is causing rapid, contemporary evolution that tends to result in a loss of extreme phenotypes, and hence a loss of the population features we wish to preserve even though population extinction has, thus far, been relatively rare. We are currently engaged in an effort to develop a proactive protection strategy for populations of threespine stickleback in both southern British Columbia and the Cook Inlet region of Alaska.

Global Environmental Change: Impacts on Stickleback
and their Watersheds

Global warming and human development are having particularly extreme effects in south central Alaska. As is the case throughout Alaska, global warming is causing changes in lake productivity, alterations in lake and stream watersheds due to impacts from beetle infestations on the dominant spruce tree species, and an increased fire hazard. All of these changes influence the ecology of the lakes and streams in which stickleback are found. Particularly of concern is an apparent dramatic increase in the productivity of the mostly oligo- and mesotrophic lakes in the region. In addition, human development is leading alteration of lakes and streams due to physical modifications of the watersheds, and also via productivity increases associated with septic systems. We have discovered that increased lake productivity is causing rapid contemporary evolution in stickleback life histories, and are attempting to understand how global warming and development affect watersheds and, in turn, the stream and lacustrine communities they support.



Clark University | Worcester, MA | 508.793.7173