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# Divergence in Thermal Physiology Could Contribute to Vertical Segregation in Intertidal Ecotypes of Littorina saxatilis

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## Abstract

Thermal stress is a potentially important selective agent in intertidal marine habitats, but the role that thermal tolerance might play in local adaptation across shore height has been underexplored. Northwest Spain is home to two morphologically distinct ecotypes of the periwinkle Littorina saxatilis, separated by shore height and subject to substantial differences in thermal stress exposure. However, despite other biotic and abiotic drivers of ecotype segregation being well studied, their thermal tolerance has not been previously characterized. We investigated thermal tolerance across multiple life history stages by employing the thermal death time (TDT) approach to determine (i) whether the two ecotypes differ in thermal tolerance and (ii) how any differences vary with life history stage. Adults of the two ecotypes differed in their thermal tolerance in line with their shore position: the upper-shore ecotype, which experiences more extreme temperatures, exhibited greater endurance of thermal stress compared with the lower-shore ecotype. This difference was most pronounced at the highest temperatures tested. The proximate physiological basis for these differences is unknown but likely due to a multifarious interaction of traits affecting different parts of the TDT curve. Differences in tolerance between ecotypes were less pronounced in early life history stages but increased with ontogeny, suggesting partial divergence of this trait during development. Thermal tolerance could potentially play an important role in maintaining population divergence and genetic segregation between the two ecotypes, since the increased thermal sensitivity of the lower-shore ecotype may limit its dispersal onto the upper shore and so restrict gene flow.

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The study of speciation in recent populations is essentially a study of the evolution of reproductive isolation mechanisms between sub-groups of a species. Prezygotic isolation can be of central importance to models of speciation, either being a consequence of reinforcement of assortative mating in hybrid zones, or a pleiotropic effect of morphological or behavioral adaptation to different environments. To suggest speciation by reinforcement between incipient species one must at least know that gene flow occurs, or have recently occurred, and that assortative mating has been established in the hybrid zone. In Galician populations of the marine snail Littorina saxatilis, two main morphs appear on the same shores, one on the upper-shore barnacle belt and the other in the lower-shore mussel belt. The two morphs overlap in distribution in the midshore where hybrids are found together with pure forms. Allozyme variation indicates that the two parental morphs share a common gene pool, although within shores, gene flow between morphs is less than gene flow within morphs. In this study, we observed mating behavior in the field, and we found that mating was not random in midshore sites, with a deficiency of heterotypic pairs. Habitat selection, assortative mating, and possibly sexual selection among females contributed to the partial reproductive isolation between the pure morphs. Sizes of mates were often positively correlated, in particular, in the upper shore, indicating size-assortative mating too. However, this seemed to be a consequence of nonrandom microdistributions of snails of different sizes. Because we also argue that the hybrid zone is of primary rather than secondary origin, this seems to be an example of sympatric reproductive isolation, either established by means of reinforcement or as a by-product to divergent selection acting on other characters.
Article
Steep clinal transitions in one or several inherited characters between genetically distinct populations are usually referred to as hybrid zones. Essentially two different mechanisms may maintain steep genetic clines. Either selection acts against hybrids that are unfit over the entire zone due to their mixed genetic origin (endogenous selection), or hybrids and parental types attain different fitness values in different parts of the cline (exogenous selection). Survival rate estimates of hybrids and parental forms in different regions of the cline may be used to distinguish between these models to assess how the cline is maintained. We used reciprocal transplants to test the relative survival rates of two parental ecotypes and their hybrids over microscale hybrid zones in the direct-developing marine snail Littorina saxatilis (Olivi) on the rocky shores of Galicia, Spain. One of the parental forms occupies upper and the other lower shores, and the hybrids are found at various proportions (1-38%) along with both parental forms in a midshore zone a few meters wide. The survival rate over one month was 39-52% of the native ecotype on upper shores, but only 2-8% for the lower-shore ecotype. In contrast, only 4-8% of the upper-shore ecotype but 53% of large (> 6 mm) and 8% of small (3-6 mm) native lower-shore ecotype survived in the lower shores. In the midshores, both the two parental ecotypes and the hybrids survived about equally well. Thus there is a considerable advantage for the native ecotypes in the upper and lower shores, while in the hybrid zone none of the morphs, hybrids included, are favored. This indicates that the dimorphism of L. saxatilis is maintained by steep cross-shore selection gradients, thus supporting the selection-gradient model of hybrid zones. We performed field and laboratory experiments that suggest physical factors and predation as important selective agents. Earlier studies indicate assortative mating between the two ecotypes in the midshore. This is unexpected in a hybrid zone maintained by selection gradients, and it seems as if the reproductive barrier compresses the hybrid zone considerably.
Article
Abstract The classification of reproductive isolating barriers laid out by Dobzhansky and Mayr has motivated and structured decades of research on speciation. We argue, however, that this classification is incomplete and that the unique contributions of a major source of reproductive isolation have often been overlooked. Here, we describe reproductive barriers that derive from the reduced survival of immigrants upon reaching foreign habitats that are ecologically divergent from their native habitat. This selection against immigrants reduces encounters and thus mating opportunities between individuals from divergently adapted populations. It also reduces the likelihood that successfully mated immigrant females will survive long enough to produce their hybrid offspring. Thus, natural selection against immigrants results in distinctive elements of premating and postmating reproductive isolation that we hereby dub “immigrant inviability”. We quantify the contributions of immigrant inviability to total reproductive isolation by examining study systems where multiple components of reproductive isolation have been measured and demonstrate that these contributions are frequently greater than those of traditionally recognized reproductive barriers. The relevance of immigrant inviability is further illustrated by a consideration of population-genetic theory, a review of selection against immigrant alleles in hybrid zone studies, and an examination of its participation in feedback loops that influence the evolution of additional reproductive barriers. Because some degree of immigrant inviability will commonly exist between populations that exhibit adaptive ecological divergence, we emphasize that these barriers play critical roles in ecological modes of speciation. We hope that the formal recognition of immigrant inviability and our demonstration of its evolutionary importance will stimulate more explicit empirical studies of its contributions to speciation.
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Article
Changes in oxygen uptake in response to stepwise changes in environmental temperature have been measured in anomuran decapod Crustacea inhabiting a subtidal habitat (Paguristes turgidus, Elassochirus tenuimanus), an intertidal habitat (Pagurus granusimanus, Pagurus hirsutisculus) and a supratidal habitat (Coenobita clypeatus, Coenobita rugosus). Individuals of each species were housed in respirometers and subjected to three rapid, progressive 5 C increases above their initial acclimation temperature, with (μM O₂/g/h) measured during a 2-3-h pause at each temperature increment. The for is correlated with habitat, with intertidal species having a of 1.4-1.6, which is significantly lower (P < .05) when compared with values of 2.1-2.4 for subtidal species and 2.6-2.7 for the supratidal forms. Intertidal hermit crabs also showed a smaller overshoot and a more rapid acclimation to abrupt temperature change compared with the other anomurans. Intertidal anomuran Crustacea are apparently adapted to maintain a comparatively stable oxygen uptake in a habitat subject to considerable variability in temperature.
Article
The origin of biological diversity, via the formation of new species, can be inextricably linked to adaptation to the ecological environment. Specifically, ecological processes are central to the formation of new species when barriers to gene flow (reproductive isolation) evolve between populations as a result of ecologically based divergent natural selection. This process of 'ecological speciation' has seen a large body of focused research in the last ten-fifteen years, and a review and synthesis of the theoretical and empirical literature is now timely. The book begins by clarifying what ecological speciation is, its alternatives, and the predictions that can be used to test for it. It then reviews the three components of ecological speciation and discusses the geography and genomic basis of the process. A final chapter highlights future research directions, describing the approaches and experiments which might be used to conduct that future work. The ecological and genetic literature is integrated throughout the text with the goal of shedding new insight into the speciation process, particularly when the empirical data is then further integrated with theory.
Article
Because of their complex life histories, different life stages of many marine invertebrates may be exposed to varying environmental challenges. Ultimately, the life stage that is least tolerant of its environment will determine the species' abundance and distribution. The intertidal copepod Tigriopus californicus lives in high intertidal pools along the Pacific coast of North America. Unlike most other invertebrates, the different life stages of T. californicus all share the same tidepool habitat. To determine physiological tolerances of various life history stages of this species, we examined responses to acute heat stress in nauplii, copepodids, and adults from 6 populations along a latitudinal gradient. Results show that early developmental stages (nauplii and copepodids) are generally more tolerant than adults. Our results contrast with the widely accepted generalization that larval forms are more sensitive to physical stressors than adults. As previously observed in adults, nauplii and copepodids from southern populations survive higher temperatures than those from northern populations. Acute heat stress was found to delay development but did not affect adult size. We hypothesize that variation in the thermal tolerance of early life stages among intertidal species reflects ecological differences in larval habitats: where larvae remain in the intertidal zone and experience the same high temperatures as adults, selection will favor high larval thermal tolerance, while in species with planktonic larvae, the buffered temperature regime of the water column might relax such selection, and thermal tolerance will be highest in the more exposed intertidal adults.
Article
Animals living in the marine intertidal zone have a suite of adaptations that allow them to survive thermal stresses associated with low tides. We hypothesized that adjustments of adult organisms to their thermal environment might be reflected in the thermal tolerances of their developing offspring (i.e, adults that survive large temperature fluctuations might produce embryos that have similarly large tolerances). Comparison of the thermal biology of developing sand dollar embryos (Dendraster excentricus) which were offspring of adults living in intertidal or subtidal habitats revealed subtle differences in effects of temperature on survival and developmental rates. Intertidal and subtidal D. excentricus showed similar fertilization success at temperatures from 7°to 19°C and could develop from fertilized egg to pluteus larva at temperatures from 7°to 26°C. Within this common tolerance range, however, subtidal animals' offspring were more likely to develop normally at lower temperatures (8°- 16°C), while the intertidal animals' offspring were more likely to develop normally at higher temperatures (22°- 26°C). There were also significant differences between subtidal and intertidal Dendraster groups in the effects of temperature on developmental rates. In particular, cleavage rates of embryos from intertidal adults remained constant or increased as temperature was raised from 7 to 15°C. In contrast, cleavage rates of embryos from subtidal adults decreased with increasing temperature. Ecological observations suggest that these differences are due to physiological acclimatization effects rather than genetic differentiation of the groups. To contrast D. excentricus with a different species that is largely confined to subtidal depths, we also examined temperature tolerances of developing sea urchin embryos (Strongylocentrotus droebachiensis). We found that its temperature tolerance during early development was slightly narrower and shifted to lower temperatures than that of D. excentricus. This correlates well with differences in habitat and reproductive season of these species and may help explain their distributions and abundances.
Article
When exposed to air, the phylogenetically distant intertidal limpets Patella granularis (Prosobranchia) and Siphonaria oculus (Pulmonata) displayed diferent levels of survival and metabolic adjustment. Siphonaria oculus lost water at a significantly higher rate, a response probably relating to its less domed shell Despite this, lethal exposure time and lethal water loss ( $LT_{50} = 158 h$ ; $LD_{50} = 59%$ ) were considerably higher than for P. granularis ( $LT_{50} = 89 h$ ; $LD_{50} = 34%$ ). Oxygen uptake rates ( $\dot{V}o_{2}$ ) for both species remained constant over 12 h in air of 100% relative humidity (RH), when water loss was presumably negligible, but declined significantly in P. granularis after longer (24 h) exposure. Desiccation at 0% RH led to a marked decline in $\dot{V}o_{2}$ in both species. The $\dot{V}o_{2}$ of S. oculus fell to as low as 18% of the initial nondesiccated rate, whereas in P. granularis $\dot{V}o_{2}$ never declined below 38% of the initial rate. When reimmersed after 12 h desiccation at 0% RH, S. oculus showed no "oxygen debt" repayment. The comparatively limited depression of aerobic metabolism of P. granularis, followed by early mortality, is interpreted as a stress-related response to impairment of gas exchange. High survivorship of S. oculus, despite drastic reduction in $\dot{V}o_{2}$ , may indicate adaptive depression of metabolic rate. The extension of vertical distribution by S. oculus further up the shore than P. granularis is discussed with regard to their respective water relations and metabolic characteristics during progressive aerial exposure.
Article
We have examined the role of stress proteins in adaptation through an interspecific study of the stress protein response in two species of Collisella limpets that occupy different intertidal habitats characterized by unique microclimates. Collisella scabra inhabits the high intertidal region, an unpredictable environment of temperature extremes. Collisella pelta lives in the more sheltered upper midtidal region. We conducted laboratory experiments to compare the temperature tolerance of each species and confirmed that C. scabra had a greater tolerance to acute heat shock. The stress protein response was also examined for both species using metabolic labeling and electrophoretic techniques. We found in C. scabra, but not in C. pelta, a highly complex group of low-molecular-weight (LMW) stress proteins (also called heat-shock proteins [hsp]) and multiple isoforms of hsp60. Other aspects of the response that also differed included (1) the temperature range at which the response was elicited, (2) the number of isoforms of hsp70 synthesized, and (3) the presence of stressproteins in the 35-40-kDa range in C. scabra. Further, the increase of radiolabel incorporation into hsp70 and the LMW stress proteins at higher temperatures relative to control temperatures was greater for C. scabra. These aspects of the stress protein response may play a role in allowing C. scabra to tolerate the temperature extremes of the high intertidal region that provides it with access to food sources not available to closely related but more temperature-sensitive species.
Article
The upper temperature tolerance of 10 commercially important South American bivalve species (Gari solida, Semele solida, Semele corrugata, Protothaca thaca, Venus antiqua, Tagelus dombeii, Ensis macha, Aulacomya ater, Choromytilus chorus and Argopecten purpuratus) off Peru and Chile was determined and compared in order to study some of the effects of El Nino. Due to higher habitat temperatures in Peru, LT50 (lethal temperatures for 50 % of an experimental population) are higher than in Chile. In Chile LT50 for 6 of 8 species studied varied only by 1.2-degrees-C. This might be explained by the similar temperatures and living conditions in the habitats of these species. Especially for Peru, observed differences in LT50 could be related to different geographical distributions. For all species temperature increases recorded during the strongest El Nino of this century (1982-83) did not exceed the temperature tolerance interval, = (difference between LT50 after 24 h and mean annual water temperature). It is noted that all species studied here are tolerant of temperature conditions occurring during moderate El Nino events.
Article
A review of chemical, fossil and functional approaches to the reconstruction of the beginning of life suggests an early role for the 'opine' pathways in providing energy for the burrowing of infaunal worms of the Precambrian era. It is concluded that biological rather than chemical factors have been the main forces for the evolution of anaerobic metabolism. -R.A.H.
Article
On raising the temperature of Thais lapillus, Littorina littorea, L. littoralis, and L. saxatilis in air and when submerged, the oxygen uptake in air is consistently higher than in water up to the temperature at which heat death occurs. With a further rise in temperature after the snail has entered heat coma two distinct respiratory patterns emerge, namely, in submerged snails the respiratory rate falls until the temperature at which death ensues, whereas in snails kept in air the respiratory rate shows an initial rise followed by a fall prior to thermal death. The reasons for these two respiratory patterns are discussed.The temperatures at which snails enter heat coma are up to 10 °C lower than those which are lethal to the species so that heat coma is considered to be a potential zonation controller. Snails on entering heat coma have the foot relaxed and consequently are liable to desiccation of the mantle cavity which in air may prove to be lethal, whereas in water, snails which enter heat coma are not exposed to the hazard of desiccation. The coma temperatures of snails in air are a few degrees higher than in water, thus giving an additional safeguard against the dangers of desiccation.The temperature tolerance of Thais and Littorina spp. varies with geographical distribution. Heat coma and lethal temperatures of snails from Cardigan Bay are slightly higher when compared with snails from the Firth of Forth than would be expected if acclimation to the temperature of the environment were the only factor involved.
Article
As ectothermic organisms, butterflies have widely been used as models to explore the predicted impacts of climate change. However, most studies explore only one life stage; to our best knowledge, none have integrated the impact of temperature on the vital rates of all life stages for a species of conservation concern. Besides, most population viability analysis models for butterflies are based on yearly population growth rate, precluding the implementation and assessment of important climate change scenarios, where climate change occurs mainly, or differently, during some seasons. Here, we used a combination of laboratory and field experiments to quantify the impact of temperature on all life stages of a vulnerable glacial relict butterfly. Next, we integrated these impacts into an overall population response using a deterministic periodic matrix model and explored the impact of several climate change scenarios. Temperature positively affected egg, pre-diapause larva and pupal survival, and the number of eggs laid by a female; only the survival of overwintering larva was negatively affected by an increase in temperature. Despite the positive impact of warming on many life stages, population viability was reduced under all scenarios, with predictions of much shorter times to extinction than under the baseline (current temperature situation) scenario. Indeed, model predictions were the most sensitive to changes in survival of overwintering larva, the only stage negatively affected by warming. A proper consideration of every stage of the life cycle is important when designing conservation guidelines in the light of climate change. This is in line with the resource-based habitat view, which explicitly refers to the habitat as a collection of resources needed for all life stages of the species. We, therefore, encourage adopting a resource-based habitat view for population viability analysis and development of conservation guidelines for butterflies, and more generally, other organisms. Life stages that are cryptic or difficult to study should not be forsaken as they may be key determinants in the overall response to climate change, as we found with overwintering Boloria eunomia larvae.
Article
This work introduces new biomimetic devices to record body temperatures of sessile intertidal animals. These waterproof devices, built around dissected circuit boards from Maxim DS1922 Thermochron iButtons, are demonstrated using intertidal limpets (Tectura persona). Data were validated by a field experiment carried out at Friday Harbor, Washington, USA. These loggers, named robolimpets, can easily be deployed to autonomously and accurately measure temperatures for long periods of time. Given that they mimic the visual aspect of real animals, they have the advantage of being inconspicuous in the intertidal environment. Their measurements not only match the temperature trajectories, but also the warming and cooling rates and daily temperature maxima and minima of live limpets. Robolimpets provide valuable data on the body temperatures experienced by intertidal animals.