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Adult Plasticity and Rapid Larval Evolution in a Recently Isolated

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Adult Plasticity and Rapid Larval Evolution in a Recently Isolated 3g~! Reference : Biol. Bull. 182 :210-220. (April, 1992) of 1 19" chz ob' poi pot Sae ar in a Recently Isolat d Barnacle Population PETER T. RAIMONDI The Marine Science Institute a Department of Biological Sciences, University of California, S nta Barbara, California 93106 Abstract. Balanus amphitrite, a common barnacle spe- entiation (Gould and Johnson, 1972 ; Berven et al., 1979; cies, was introduced into the landlocked Salton Sea in Falconer, 1989); implicitly assumed in both cases is that, 1943 or 1944. In 1949, Balanus amphitrite from the Salton within a species, all individuals share a common ancestor Sea was classified as the subspecies, Balanus amphitrit and, therefore, are derived from the same ancestral ge- saltonensis, based upon morphological differences be- notype. First, populations may evolve differently (evolu- tween Salton Sea and coastal individuals . This classifi- tion). Second, even when the gene frequencies of two cation was maintained following an investigation of the populations do not differ, phenotypic differences may re- Balanus amphitrite complex in 1975. Such a designation sult from plasticity in some traits (phenotypic plasticity; implies that the morphological divergence is underlain b see Smith-Gill, 1983 ; West-Eberhard, 1989 for a discus- genetic differences. Using field and laboratory transplan- sion of the forms of phenotypic plasticity) . The two pro- tations, I tested the alternative hypothesis that the ob- cesses may also interact to produce phenotypic variation served morphological divergence in the adult stage o among populations . Balanus amphitrite was the result of phenotypic plasticity . The distinction between phenotypic differentiation by The results show that the divergence in the examined adul evolutionary mechanisms and differentiation resulting characters is in fact due to environmentally induced phe- from phenotypic plasticity cannot be made on the grounds notypic plasticity. There were also phenotypic difference that the latter has a non-genetic basis (West-Eberhard, between larvae from the Salton Sea and those from 1989). Phenotypically plastic responses (to the environ- habitats that only became apparent during experimen- ment) have as much genetic basis as do other less plastic tation with the adult stage. Here, however, experimental characters, and plasticity is therefore a trait subject to results suggest that the divergence was due to an evolu evolutionary change (Bradshaw, 1965 ; Williams, 1966 ; tionary process, probably selection . These results al Schlichting, 1986; Macdonald et al., 1988; West-Eberhard, provide the basis for two slightly precautionary conclu- 1989). The distinction is simply that evolution is a char- sions: (1) the observation that individuals living in typi acteristic of populations, whereas plasticity is a charac- and novel habitats differ cannot even weakly indicate teristic of individuals (after Lewontin, 1957). Thus, for cause for the difference, and (2) a consideration of th populations in which individuals exhibit no plasticity, divergence of populations is incomplete if all of the lif phenotypic modification as a response to the environment history stages of the organism are not studied . is possible only at the level of the population (across gen- erations). In contrast, for populations in which individuals t Introduction exhibit plastic characters, phenotypic modification in re- sponse to the environment is possible at the level of the One of the continuing challenges in evolutionary ecol individual (within a generation) . t= ogy is to determine the genetic contribution to phenotype Either as untidy noise in complicates genetic systems variation among populations . Two general, and non-in as it was once regarded (see West-Eberhard, 1989), or as dependent processes can cause such phenotypic differ a selectable trait (Schlichting, 1986), plasticity is important to measure. This is because without determining the con- Received 13 May 1991 ; accepted 6 January 1992 . tribution of phenotypic plasticity, the adaptive canoe of phenotypic variation cannot be assessed (Berven et al. taken from the field . However, Newman and Abbott 1979). In this study I investigated whether evolutio (1980) suggested that because the Salton Sea form was change or phenotypic plasticity was responsible for th also found in a population from Wilmington Harbor (Pa- observed phenotypic variation between two California cific coast), the difference was ecotypic . Flowerdew (1985) populations of the barnacle, Balanus amphitrite. On has recently recommended, based upon an electrophoretic population was from a typical coastal (harbor) habitat i investigation of 31 alleles at 11 loci, that the subspecies San Diego, California, the other was recently isolated i designation for the Salton Sea population be removed. a novel environment, the Salton Sea . He found that the values from both indices of genetic The Salton Sea is a recently formed landlocked identity (I) and genetic distance (D) were in the range of of saline water, the largest body of water in California. I variation expected between conspecific populations (Nei, average size is 55 by 24 kilometers, but the dimensio s 1972). He also concluded that there was no "significant vary considerably (Carpelan, 1961 a) . The genesis and r genetic differentiation" ofBalanus amphitrite saltonensis cent history of the Salton Sea have created an environme t from Balanus amphitrite amphitrite . This implies that no that is in many ways different from an open marine e evolutionary divergence could have occurred between the vironment (Carpelan, 1961b) and yet supports a simp populations, which is incorrect. Nonsignificant I and D but fascinating, community of introduced marine speci values should only be viewed as not refuting the null hy- In 1904-1905, a series of floods on the Colorado and G' a pothesis that there is no divergence between populations rivers breached the headworks of an irrigation chann for the tested alleles (Richardson et al., 1986). Indeed, For two years these rivers, which normally drain into t e there are cases of apparently separate (good) species Gulf of California, emptied into the Salton Sink, a la B- showing no electrophoretic divergence (Avise et al., 1975). locked sub-sea level basin in southeastern California, a d My initial interest was to determine whether the ob- thus formed the Salton Sea. Since 1907, when the h d- served morphological divergence between Salton Sea and works were repaired, the level of the Salton Sea has n coastal adults (Henry and Mclaughlin, 1975) was due to maintained by irrigation water, and its salinity has ri n environmental factors. As the samples used in this initial from 3.65% (Carpelan, 1961b) to about 43%o (Ano study came from field collections, there was no way to mous, 1989) ; the latter value is between 5 and 8%o gr er determine the contribution of the environment to the di- than is typical for ocean water . The visibility (usually ss vergence. In the present study I made no attempt to eval- than 1 m in the Salton Sea), ionic composition, chlori ty, uate any adult character other than those that had been pH, dissolved oxygen, and temperature fluctuations ( 0- described as differing between the two populations. This 36°C) of Salton Sea water differ from those of ocean w ter was because : (1)1 was interested in determining the basis (Carpelan, 1961b; Raimondi, pers. obs.); because it i an for the differentiating characters, and (2) the selection of inland body of water, tidal fluctuations in the Salton ea additional characters would have been largely unmoti- are trivial . vated, because, unlike larvae (see following), when adults Balanus amphitrite was first noticed in the Salton Sea from different populations were reared under experimen- in about 1943-1944 . Apparently B. amphitrite individ s tal conditions, they could not be distinguished . were transported from the San Diego area by air du ng While evaluating the mechanisms determining adult Naval exercises, as adults on mooring buoys or r pes morphological divergence, I found a number of differences (Cockerall, 1945 ; Newman and Abbott, 1980), or as ae in the larvae of the two populations . The basis of these in the bilge water of Naval flying boats (Hilton, 1945 By differences was also examined . late 1944 they were ubiquitous: ". they were dy multiplying so fast that a stick or board only had to in Materials and Methods the water a few days before a crust of minute barn cles Study organism, sites, and general methods started to form ." (from Hilton, 1945) . "Barnacles now seem to outnumber all other forms of life, both verte rate Balanus amphitrite is a moderately sized bay barnacle and invertebrate, found in the Salton Sea." (from ock- [average basal diameter is between 15 and 20 mm (New- erall, 1945) . man and Abbott, 1980)), with a virtually world-wide dis- In 1949, the Salton Sea population was descn as tribution (Henry and Mclaughlin, 1975) . Like most the subspecies Balanus amphitrite saltonesis (R gers, thoracican barnacles, it is a simultaneous hermaphrodite 1949). Subspecific designation was supported by a ono- (Strathmann, 1987), and fertilized eggs are brooded in the graph by Henry and Mclaughlin (1975) on the acles mantle cavity of the parent until .they become at least of the Balanus amphitrite complex; the authors stin- stage one nauplius larvae, when tlQeyqre expelled into the guished between Balanus amphitrite amphitrite an Ba- water. In acorn barnacles such as Balanus amphitrite, lanus amphitrite saltonensis on the basis of a multiv ate there are typically seven larval stages (Strathmann, 1987) : analysis of 15 morphological characters of indi 'duals six naupliar stages (feeding) followed b the final cyprid Y 212 P. T. ONDI stage (non-feeding) . All stages are potentially planktonic, cm clay tiles in the laboratory and raised to maturity on but stage one nauplii will often stay within ;the mantle those tiles in two environments : "lab," and "lagoon" (the cavity of the parent, making stage two nauplii the first rationale for having two experimental habitats is given planktonic stage (Raimondi, pers. obs.). below). The density of settlers was about 1 cm-2 .
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