Richard K. Grosberg

Strong genetic clines and geographical variation in gene flow in the rocky intertidal barnacle Balanus glandula

A long‐standing issue in marine biology is identifying spatial scales at which populations of sessile adults are connected by planktonic offspring. We examined the genetic continuity of the acorn barnacle Balanus glandula, an abundant member of rocky intertidal communities of the northeastern Pacific Ocean, and compared these genetic patterns to the nearshore oceanography described by trajectories of surface drifters. Consistent with its broad dispersal potential, barnacle populations are genetically similar at both mitochondrial (cytochrome oxidase I) and nuclear (elongation factor 1‐alpha) loci across broad swaths of the species’ range. In central California, however, there is a striking genetic cline across 475 km of coastline between northern and southern populations. These patterns indicate that gene flow within central California is far more restricted spatially than among other populations. Possible reasons for the steep cline include the slow secondary introgression of historically separated populations, a balance between diversifying selection and dispersal, or some mix of both. Geographic trajectories of oceanic drifters closely parallel geographical patterns of gene flow. Drifters placed to the north (Oregon; ∼44°N) and south (Santa Barbara, California; ∼34° N) of the cline disperse hundreds of kilometres within 40 days, yet over the long‐term their trajectories never overlapped. The lack of communication between waters originating in Oregon and southern California probably helps to maintain strong genetic differentiation between these regions. More broadly, the geographical variation in gene flow implies that focusing on species‐level averages of gene flow can mask biologically important variance within species which reflects local environmental conditions and historical events.

The Evolution of Allorecognition Specificity in Clonal Invertebrates

Sessile, clonal invertebrates frequently encounter conspecifics as they grow over hard substrata and compete for space. Allorecognition systems mediate the nature and outcomes of these encouters by controlling somatic compatibility (fusion versus nonfusion) and agonistic behavior (aggression versus nonaggression). In general, clonemates (and sometimes close relatives) can fuse somatically, whereas more distant relatives are incompatible. Many anthozoan and hydrozoan cnidarians behave passively when in contact with clonemates and close kin, but fight aggressibely when contacting more distant relatives. This high degree of allorecognition specificity, when considered togehter with the few available data on the formal genetics of allorecognition, suggests that levels of polymorphism at allorecognition loci (i.e., allotypic variation) exceed by perhaps an order of magnitude the levels typical of other polymorphic loci. In this paper, I evaluate the strengths and weaknesses of the selectionist and nonselectionist theories that have been proposed to account for the evolution and persistence of allotypic polymorphism. It remains difficult to accept or reject any of these hypotheses in the absence of detailed empirical information concerning levels and patterns of allelic variation at allorecognition loci. Nevertheless, mathematical considerations and the available data together suggest that frequency-dependent or spatially variable selection are the strongest candidates for the maintenance of allotypic variation. Although the pleiotropic effects of allorecognition loci (e.g., the regulation of gametic compatibility or pathogenic defense) could maintain allotypic variation, pleiotropy by itself does not account for the widespread evolution of aggressive behavior and somatic compatibility conditioned by allotypic similarity. It is theoretically possible that frequency-dependent selection acting at the level of the individual maintains allotypic polymorphism by restricting somatic fusion; it is less clear how individual selection maintains allotypic variation through the regulation of agonistic behavior.

Intertidal Zonation of Barnacles: The Influence of Planktonic Zonation of Larvae on Vertical Distribution of Adults

The nonoverlapping vertical distributions of sessile species in the marine intertidal are usually considered to result from two interacting factors: (1) broadly restricted settlement of juveniles in the vertical horizon, and (2) postsettlement mortality which affects species differently. Investigated here is the role of larval behavior in molding the zonation of the acorn barnacles Balanus glandula and Balanus crenatus. I document the vertical distributions of: (a) adults, (b) newly settled spat, and (c) planktonic cyprid larvae. The data show that the vertical distribution of adults is a reflection of the vertical zonation of cyprids in the plankton and settlement patterns of spat. Although postsettlement mortality and substratum selection occur, presettlement behavior can strongly influence vertical zonation of sessile organisms. See full-text article at JSTOR

Genetic diversity, asymmetrical aggression, and recognition in a widespread invasive species

The evolution and persistence of cooperative social units depends on the ability to distinguish group members from nonmembers. The precision of discrimination, in turn, relies on variation in the labels that individuals use to recognize group members. However, this same variation can be selected against if individuals that are rejected as nonmembers incur a high cost. Here we provide evidence that selection against individuals from genetically diverse groups has contributed to the formation of the unicolonial colony structure that characterizes introduced populations of the invasive Argentine ant (Linepithema humile). Studies in both the laboratory and the field showed that individuals from less genetically diverse colonies attack individuals from more diverse colonies and that attackers survived agonistic encounters more than six times as often as recipients of aggression. This selection, in concert with reductions in genetic diversity after a founder event, likely creates a barrier to the establishment of new, genetically diverse introductions from the native range and may reduce genetic diversity within established populations in the introduced range.

LIMITED DISPERSAL AND PROXIMITY-DEPENDENT MATING SUCCESS IN THE COLONIAL ASCIDIAN BOTRYLLUS SCHLOSSERI

Although the propagules of many sessile organisms have the capacity to disperse over large distances, dispersal is often spatially restricted. In this paper, I document, using a combination of mark/recapture techniques and histocompatibility assays, dispersal distance of the planktonic larvae of the sessile, colonial sea squirt Botryllus schlosseri. Both of these methods indicate that most larvae remain within a meter of their birthplace. Such limited dispersal should lead to increased matings among relatives, and the potential for inbreeding depression. However, the success of: 1) fertilization, 2) embryogenesis, and 3) larval metamorphosis all decrease as distance between mated colonies increases. The spatial scale over which this decrease in mating success occurs is concordant with the estimates of dispersal distance based on the larval mark/recapture data and histocompatibility assays. Taken together, these results imply that inbreeding depression is not a necessary consequence of limited dispersal and consanguineous matings in B. schlosseri.

Contrasting demographic history and phylogeographical patterns in two Indo-Pacific gastropods

Marine species with ranges that span the Indo‐Australian Archipelago (IAA) exhibit a range of phylogeographical patterns, most of which are interpreted in the context of vicariance between Indian and Pacific Ocean populations during Pliocene and Pleistocene low sea‐level stands. However, patterns often vary among ecologically similar taxa, sometimes even within genera. This study compares phylogeographical patterns in two species of highly dispersive neritid gastropod, Nerita albicilla and Nerita plicata, with nearly sympatric ranges that span the Indo‐Pacific. Mitochondrial COI sequences from > 1000 individuals from 97 sites reveal similar phylogenies in both species (two divergent clades differing by 3.2% and 2.3%, for N. albicilla and N. plicata, respectively). However, despite ecological similarity and congeneric status, the two species exhibit phylogeographical discordance. N. albicilla has maintained reciprocal monophyly of Indian and Pacific Ocean populations, while N. plicata is panmictic between oceans, but displays a genetic cline in the Central Pacific. Although this difference might be explained by qualitatively different demographic histories, parameter estimates from three coalescent models indicate that both species have high levels of gene flow between demes (2Nem > 75), and share a common history of population expansion that is likely associated with cyclical flooding of continental shelves and island lagoons following low sea‐level stands. Results indicate that ecologically similar, codistributed species may respond very differently to shared environmental processes, suggesting that relatively minor differences in traits such as pelagic larval duration or microhabitat association may profoundly impact phylogeographical structure.

For adults only? Supply-side ecology and the history of larval biology.

When ecologists study organisms with multiphasic life cycles, they must often confront the problem of which phase to scrutinize. In principle, the dynamics and interactions of all stages could play a major role in the regulation of adult populations and species assemblages. In practice, however, the roles of larger and more sedentary phases - being easier to count and manipulate than motile propagules - have been emphasized. Nonetheless, several recent studies on the small, dispersing larval phase of marine invertebrate life cycles reach the conclusion that the spatial distribution and supply of propagules can control the distribution and abundance of populations of benthic adults. To some, the present emphasis on planktonic propagules amounts to a resurrection of ideas developed during a long and rich history of larval biology. To others, studies of demographic and ecological connections between larval and adult populations represent a substantial revision of ecological paradigms.

SPERM-MEDIATED GENE FLOW AND THE GENETIC STRUCTURE OF A POPULATION OF THE COLONIAL ASCIDIAN BOTRYLLUS SCHLOSSERI

The genetic structure of populations of sessile and sedentary organisms is often characterized by microgeographic differentiation in gene frequencies and deviations from panmixia. In many terrestrial botanical systems, restricted gene flow via seed and pollen dispersal may have an important role in promoting such genetic patterns. Until recently, however, limited dispersal of the sexual propagules of benthic invertebrates has not been considered to play a comparable role in aquatic systems. Based on paternity analyses in the field using rare allozyme markers, it appears that concentrations of sibling sperm of the sessile, colonial ascidian Botryllus schlosseri decline rapidly within 50 cm of a source colony. In combination with spatially restricted dispersal of brooded larvae, limited dispersal of sperm should enhance the potential for genetic diversification and inbreeding. However, analysis of allelic and genotypic frequencies at three independent, polymorphic allozyme loci using F‐statistics provides little evidence for microgeographic variation in gene frequencies. This lack of differentiation can be explained in terms of the absolute number (rather than concentration) of gametes and larvae dispersing from a point source, which—depending on diffusion and geometric assumptions—may actually increase with distance. In contrast to the absence of differentiation, levels of inbreeding are high, even within the confines of 25 times 25–cm quadrats. The absence of genetic diversification and presence of inbreeding caution against inferring levels and causes of gene flow from indirect analysis of genetic structure and, conversely, making predictions about genetic and breeding structure based solely on direct analysis of gene flow.

The Timing of Sexual Maturity in Clonal Animals

The indeterminate growth potential of many clonal organisms sets them apart from solitary organisms on two demographic counts: (1) fecundity may increase indeterminately and (2) the age-specific probability of genet mortality may decline expo- nentially with size. In contrast to most solitary organisms, the fecundity benefits of post- poning sexual reproduction are not necessarily offset by a rapidly increasing risk of mortality among clonal organisms with indeterminate growth. We examined patterns and causes of variation in the timing of sexual maturity in clonal organisms through experimental ma- nipulations of two phyletically distinct, sessile, colonial marine invertebrates. In the bryo- zoan Membranipora membranacea, both crowding by conspecifics and simulated grazing triggered the onset of sexual maturity. Within a population of the colonial ascidian Botryllus schlosseri, there are two genetically determined life history morphs. The semelparous morph grows determinately and reproduces at a fixed size. The iteroparous morph can grow indeterminately and reproduces when extrinsic factors (e.g., substratum limitation) inter- vene. Analysis of the literature on other sessile, clonal taxa suggests that reproduction is timed differently for annual, indeterminately growing, and perennial, determinately growing, taxa. Many annual clonal species show extreme flexibility in size of first reproduction and reproduce over a wide range of sizes depending on extrinsic factors. Many long-lived clonal species delay reproduction throughout unfavorable conditions until attaining some mini- mum size. Beyond this size, a combination of age and extrinsic factors appears to modify the actual size at first reproduction.

Life-history variation within a population of the colonial ascidian Botryllus schlosseri. I: The genetic and environmental control of seasonal variation

Many empirical analyses of life‐history tactics are based on the assumption that demographic variation ought to be greatest among populations or species living in different environments. However, in a single population of the sessile colonial sea squirt Botryllus schlosseri, there are two discrete life‐history morphs. Semelparous colonies are characterized by a) death immediately following the production of a single clutch, b) early age at first reproduction, c) rapid growth to first reproduction, and d) high reproductive effort. In contrast, iteroparous colonies a) produce at least three clutches before dying, b) postpone sexual reproduction until they are nearly twice the age of semelparous colonies, c) grow at about half the rate of semelparous colonies, and d) invest roughly 75% less in reproductive effort than semelparous colonies. Semelparous colonies numerically dominate the population through midsummer; later in the summer, iteroparous colonies are most numerous. Field and laboratory common‐garden experiments, along with breeding studies, indicate that the demographic differences between the morphs are genetically determined. Consequently, the seasonal switch from dominance by semelparous colonies to dominance by iteroparous colonies may be an evolved response to a seasonally changing environment. On theoretical grounds, temporal variation in selection is thought to play a relatively unimportant role in maintaining genetic polymorphism; nonetheless, the seasonally recurrent life‐history polymorphism shown in this study indicates that temporal variation in selection can lead to the maintenance of genetic polymorphism for traits strongly affecting fitness.