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Absence of Countergradient and Cogradient Variation in an Oceanic Silverside, the California Grunion Leuresthes Tenuis

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Absence of Countergradient and Cogradient Variation in an Oceanic Silverside, the California Grunion Leuresthes Tenuis Vol. 461: 175–186, 2012 MARINE ECOLOGY PROGRESS SERIES Published August 8 doi: 10.3354/meps09802 Mar Ecol Prog Ser Absence of countergradient and cogradient variation in an oceanic silverside, the California grunion Leuresthes tenuis Elizabeth E. Brown*, Hannes Baumann, David O. Conover School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, New York 11794-5000, USA ABSTRACT: Spatial adaptations that maximize a species’ fitness in its local environment, particu- larly in the form of countergradient variation (CnGV = genotypic influences counteract environ- mental effects on trait variation) and cogradient variation (CoGV = genotypic influences accentu- ate environmental plasticity), have been documented in many estuarine and anadromous fishes. However, their prevalence in more oceanic fishes, where extensive gene flow and reduced envi- ronmental selection may preclude local adaptation, remains unclear. If oceanic species lack genetic structure, they may be limited in their ability to adapt to global climate change. We exam- ined the potential for adaptation in oceanic fishes by testing whether an oceanic silverside, the California grunion Leuresthes tenuis, displays CnGV in growth capacity and CoGV in vertebral number across a latitudinal gradient as found in estuarine silversides. Common garden experi- ments revealed that reaction norms for growth in response to temperature differed little among 3 L. tenuis populations from different latitudes. Growth rates of wild adult L. tenuis measured from scale analysis suggested that growth may be slightly faster at more southern latitudes, likely due to environmental variation. Mean vertebral number in wild L. tenuis, determined from radio- graphs, were nearly identical for all populations. Overall, our results did not provide evidence for spatial adaptations in these traits of L. tenuis, in contrast to the strong patterns of latitudinal trait adaptation in other, more estuarine silversides. This study provides support for the finding that higher gene flow levels and weaker environmental selection pressures of oceanic species limit local adaptation. KEY WORDS: Latitudinal gradient · Gene flow · Adaptation · Growth capacity · Vertebral number · Climate change · Environmental selection Resale or republication not permitted without written consent of the publisher INTRODUCTION tion to natural environmental variation. Additionally, this knowledge may provide clues to potential evolu- Species distributed across broad environmental tionary responses to temporal environmental change gradients, such as those that occur along latitudes or (Deutsch et al. 2008, Baumann & Conover 2011), altitudes, often exhibit phenotypic variation in which is becoming increasingly important to under- physio logical and morphological traits. This variation stand as global climate change may alter species dis- is likely due to a combination of environmental in - tributions and life histories. fluences on phenotypic expression (i.e. phenotypic Spatial adaptations have been found in a number plasticity) and adaptive genetic variations that maxi- of marine species, particularly in coastal fishes mize a species’ fitness in its local environment (reviewed by Conover et al. 2009). However, the (Conover et al. 2009). Examination of the co-variation majority of these cases are estuarine or anadromous between genetic and environmental influences fishes, while fewer examples involve more oceanic within species may reveal spatial patterns of adapta- fishes (Conover et al. 2009). Therefore it remains *Email: [email protected] © Inter-Research 2012 · www.int-res.com 176 Mar Ecol Prog Ser 461: 175–186, 2012 unclear whether local adaptations are common in Yamahira et al. 2006, Baumann et al. 2012). Higher oceanic fishes as well. For estuarine fishes, mixing vertebral numbers at northern latitudes may be among populations is likely to be partially restricted, adaptive for enhanced swimming abilities in colder, hence enabling local adaptation (Conover et al. more viscous waters (Swain 1992a). 2006), while broad-scale dispersal and high levels of Although fewer, some cases of CnGV and CoGV mixing may limit the extent to which local adapta- have also been documented for oceanic species tions can evolve in oceanic species (Felsenstein 1976, (reviewed by Conover et al. 2009). For example, Slatkin 1987). However, strong selection pressures Atlantic cod Gadus morhua, displays CnGV in may, in some cases, override high gene flow, thereby growth patterns similar to those of estuarine silver- allowing adaptations to exist (Schneider et al. 1999, side fishes (Salvanes et al. 2004). Two flatfish species, Saint-Laurent et al. 2003). Additionally, the more turbot and halibut, have also been shown to exhibit homogenous environments of oceanic fishes com- CnGV in growth (Imsland et al. 2000, Jonassen et al. pared to estuarine fishes may result in weaker envi- 2000), and a reef fish, the neon damselfish, was found ronmental selection pressures, also making spatial to show CnGV in egg size and number (Kokita 2003), adaptations less likely. If oceanic species tend to lack although in these species mixing may be more lim- genetic structure, they may be limited in their ability ited compared to other oceanic fishes (Fairbairn to respond to climate change, since populations may 1981, Grant et al. 1984, Diakov 1998, Foss et al. 1998, not be able to respond differently across their range Shulman 1998). (Garcia-Ramos & Kirkpatrick 1997, Lenormand 2002). To better understand the effects of oceanic versus In estuarine and anadromous fishes, as well as estuarine life history on the occurrence of local adap- many other species, 2 commonly documented types tation, we studied spatial patterns of genetic varia- of spatial adaptation patterns are countergradient tion in growth capacity and vertebral number in an (CnGV) and cogradient variation (CoGV) (reviewed oceanic member of the silverside family, the Califor- by Conover et al. 2009). CnGV occurs when individ- nia grunion Leuresthes tenuis. L. tenuis has a similar uals with different genotypes are distributed across life history to other silversides, but adults spend the environment such that genetic influences on trait their life in the coastal ocean and spawn on ocean- variation oppose environmental influences, thereby front beaches, instead of the intertidal zone of resulting in diminished phenotypic expression across semi-enclosed bays and estuaries (Walker 1952, the environmental gradient (Levins 1968). In con- Esch meyer et al. 1983). Population studies of L. trast, CoGV occurs when individuals with different tenuis suggest that the species exhibits panmixia, genotypes are distributed across an environmental with high mixing and little divergence among popu- gradient such that genetic and environmental in - lations (Gaida et al. 2003, Johnson et al. 2009). fluences are reinforcing and thus increasing over - Absence of local adaptation in growth and vertebral all phenotypic variation (Levins 1969, Conover & number of L. tenuis would suggest that oceanic spe- Schultz 1995). CnGV is often observed for physiolog- cies are less likely to show local adaptations than ical traits, while CoGV is more common for morpho- estuarine fishes. Conversely, if local adaptation pat- logical traits (Conover et al. 2009). terns can be detected in L. tenuis, it would confirm For instance, estuarine silverside fishes (Atherinop- the ubiquity and importance of adaptive trait varia- sidae) along the Atlantic (Menidia menidia and M. tion even in species considered to have high popula- peninsulae) and Pacific (Atherinops affinis) coasts of tion mixing. North America display CnGV in growth capacity, To measure plastic and genetic trait variation in whereby northern populations show higher genetic Leuresthes tenuis, we used common garden experi- growth capacities (= temperature-specific growth ments, raising offspring from populations sampled at rate at unlimited food) compared to more southern multiple latitudes under the same environmental populations. This enables them to compensate for conditions. Such experiments reveal the genetic reduced growing seasons and colder average tem- component of differences in trait reaction norms peratures that occur at high versus low latitudes among populations. Population trait reaction norms (Conover & Present 1990, Yamahira & Conover 2002, that are parallel but differ in elevation in rank order Baumann & Conover 2011). In addition, vertebral with their location across a natural gradient indicate number increases with latitude in Atlantic and a CnGV or CoGV pattern (Conover et al. 2009). Pacific silversides (Jordan’s Rule; Jordan 1891), due Additionally, we measured phenotypic variation in to reinforcing environmental and genetic influences, vertebral number and growth in wild L. tenuis representing a CoGV pattern (Billerbeck et al. 1997, populations. Brown et al.: Absence of CnGV and CoGV in grunion 177 MATERIALS AND METHODS tions were made only at sites P1 and P2 due to a lack of spawning fish at site P3. Mature L. tenuis were Study species collected by hand during their beach spawning runs and immediately strip-spawned on the beach. Leuresthes tenuis (Atherinopsidae) is commonly Twelve to 20 females and more than 20 males were found along the North American Pacific coast from used for strip-spawning, except for the northernmost Punta Abreojos, Mexico (26.7° N) to Point Concep- population where a smaller spawning run dictated tion, California, USA (34.5° N)
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