Pushed waves, trailing edges, and extreme events: Eco-evolutionary dynamics of a geographic range shift in the owl limpet, Lottia gigantea.

As climatic variation re-shapes global biodiversity, understanding eco-evolutionary feedbacks during species range shifts is of increasing importance. Theory on range expansions distinguishes between two different forms: "pulled" and "pushed" waves. Pulled waves occur when the source of the expansion comes from low-density peripheral populations, while pushed waves occur when recruitment to the expanding edge is supplied by high-density populations closer to the species' core. How extreme events shape pushed/pulled wave expansion events, as well as trailing-edge declines/contractions, remains largely unexplored. We examined eco-evolutionary responses of a marine invertebrate (the owl limpet, Lottia gigantea) that increased in abundance during the 2014-2016 marine heatwaves near the poleward edge of its geographic range in the northeastern Pacific. We used whole-genome sequencing from 19 populations across >11 degrees of latitude to characterize genomic variation, gene flow, and demographic histories across the species' range. We estimated present-day dispersal potential and past climatic stability to identify how contemporary and historical seascape features shape genomic characteristics. Consistent with expectations of a pushed wave, we found little genomic differentiation between core and leading-edge populations, and higher genomic diversity at range edges. A large and well-mixed population in the northern edge of the species' range is likely a result of ocean current anomalies increasing larval settlement and high-dispersal potential across biogeographic boundaries. Trailing-edge populations have higher differentiation from core populations, possibly driven by local selection and limited gene flow, as well as high genomic diversity likely as a result of climatic stability during the Last Glacial Maximum. Our findings suggest that extreme events can drive poleward range expansions that carry the adaptive potential of core populations, while also cautioning that trailing-edge extirpations may threaten unique evolutionary variation. This work highlights the importance of understanding how both trailing and leading edges respond to global change and extreme events.

On the importance of habitat continuity for delimiting biogeographic regions and shaping richness gradients.

The formation and maintenance of biogeographic regions and the latitudinal gradient of species richness are thought to be influenced, in part, by the spatial distribution of physical habitat (habitat continuity). But the importance of habitat continuity in relation to other variables for shaping richness gradients and delimiting biogeographic regions has not been well established. Here, we show that habitat continuity is a top predictor of biogeographic structure and the richness gradient of eastern Pacific rocky shore gastropods (spanning c. 23 000 km, from 43°S to 48°N). Rocky shore habitat continuity is generally low within tropical/subtropical regions (compared to extratropical regions), but particularly at biogeographic boundaries where steep richness gradients occur. Regions of high rocky shore habitat continuity are located towards the centres of biogeographic regions where species turnover tends to be relatively low. Our study highlights the importance of habitat continuity to help explain patterns and processes shaping the biogeographic organisation of species.

Exploring the universal ecological responses to climate change in a univoltine butterfly.

Animals with distinct life stages are often exposed to different temperatures during each stage. Thus, how temperature affects these life stages should be considered for broadly understanding the ecological consequences of climate warming on such species. For example, temperature variation during particular life stages may affect respective change in body size, phenology and geographic range, which have been identified as the "universal" ecological responses to climate change. While each of these responses has been separately documented across a number of species, it is not known whether each response occurs together within a species. The influence of temperature during particular life stages may help explain each of these ecological responses to climate change. Our goal was to determine if monthly temperature variation during particular life stages of a butterfly species can predict respective changes in body size and phenology. We also refer to the literature to assess if temperature variability during the adult stage influences range change over time. Using historical museum collections paired with monthly temperature records, we show that changes in body size and phenology of the univoltine butterfly, Hesperia comma, are partly dependent upon temporal variation in summer temperatures during key stages of their life cycle. June temperatures, which are likely to affect growth rate of the final larval instar, are important for predicting adult body size (for males only; showing a positive relationship with temperature). July temperatures, which are likely to influence the pupal stage, are important for predicting the timing of adult emergence (showing a negative relationship with temperature). Previous studies show that August temperatures, which act on the adult stage, are linked to range change. Our study highlights the importance of considering temperature variation during each life stage over historic time-scales for understanding intraspecific response to climate change. Range edge studies of ectothermic species that have annual life cycles, long time-series occurrence data, and associated temperature records (ideally at monthly resolutions) could be useful model systems for intraspecific tests of the universal ecological responses to climate change and for exploring interactive effects.

The ecological and evolutionary consequences of tropicalisation.

Tropicalisation is a marine phenomenon arising from contemporary climate change, and is characterised by the range expansion of tropical/subtropical species and the retraction of temperate species. Tropicalisation occurs globally and can be detected in both tropical/temperate transition zones and temperate regions. The ecological consequences of tropicalisation range from single-species impacts (e.g., altered behaviour) to whole ecosystem changes (e.g., phase shifts in intertidal and subtidal habitats). Our understanding of the evolutionary consequences of tropicalisation is limited, but emerging evidence suggests that tropicalisation could induce phenotypic change as well as shifts in the genotypic composition of both expanding and retracting species. Given the rapid rate of contemporary climate change, research on tropicalisation focusing on shifts in ecosystem functioning, biodiversity change, and socioeconomic impacts is urgently needed.

Anthropogenic harvesting pressure and changes in life history: insights from a rocky intertidal limpet.

The importance of large breeding individuals for maintaining the health of marine fish and invertebrate populations has long been recognized. Unfortunately, decades of human harvesting that preferentially remove larger individuals have led to drastic reductions in body sizes of many of these species. Such size-selective harvesting is particularly worrisome for sequentially hermaphroditic species where the larger size classes are composed primarily of one sex. Whether these species can maintain stable sex ratios under sustained harvesting pressure depends on the level of plasticity of their life-history traits. Here, we show that populations of a marine limpet (Lottia gigantea) can adjust a fundamental aspect of their life history (the timing of sex change) when subjected to size-selective harvesting. As predicted by theoretical models, individuals from harvested populations change sex at smaller sizes and grow at slower rates compared to individuals from protected populations. In addition, the relative size at which the change from male to female occurs remains constant (~0.75; size at sex change/maximum size) across populations, regardless of harvesting pressure. Our results show that population-level demographic and life-history data, in conjunction with existing theory, can be sufficient to predict the responses of sequential hermaphrodites to harvesting pressure. Furthermore, they suggest such species can potentially adapt to size-selective harvesting.

Intraspecific plasticity and trans-generational adaptation of reproductive traits and early development in a temperate marine neogastropod.

Climate warming is altering the distribution of species, producing range shifts and promoting local extinctions. There is an urgent need to understand the underlying mechanisms that influence the persistence of populations across a species' distribution range in the face of global warming. Ocenebra erinaceus is a marine gastropod that exhibits high intraspecific variability in maternal investment and physiological capacity during early stages, which suggests local adaptation to natal environmental conditions. In this study, reproductive traits and trans-generational adaptation were measured in two subtidal populations: one from the middle (the Solent, UK) and another towards the southern end of their geographic distribution (Arcachon, France). Local adaptation was evaluated with a transfer experiment (i.e. Arcachon females transferred to Solent thermal conditions) and trans-generational adaptation was evaluated in the thermal tolerance response of embryos exposed to temperatures between 10 and 20 °C. This study shows that both populations have similar fitness; however, there are adaptive costs to live under their natal location, resulting in trade-offs between reproductive traits. Transferred females show lower reproductive output, which suggests that females are maladapted to live under a new environment. The trans-generational experiment demonstrates contrasting thermal tolerance ranges between populations. Adaptation to local thermal conditions was observed in transferred embryos, showing poor performance and high mortalities under the new environment. Our results provide a better understanding of intraspecific differences and adaptations across a species' distribution range and provide insights into how climate warming will impact encapsulated species exhibiting location-specific adaptation.

The role of temperature on the aerobic response of encapsulated embryos of Ocenebra erinaceus (Neogastropoda, Muricidae): A comparative study between two populations.

Climate warming can affect the developmental rate and embryonic survival of ectothermic species. However, it is largely unknown if the embryos of populations from different thermal regimes will respond differently to increased warming, potentially due to adaptations to natal environmental conditions. The effects of temperature on respiration rates and oxygen content of the intracapsular fluid were studied during the intracapsular development of Ocenebra erinaceus in two subtidal populations, one from the middle of their geographic distribution, the Solent, UK and another towards the southern portion: Arcachon, France. In this laboratory study, embryos were exposed to temperatures in the range of 14-20 °C. The encapsulation period for both populations was shorter at higher temperatures and intracapsular oxygen availability decreased as development progressed. However, the embryonic aerobic response differed between populations. Encapsulated embryos from the southern population (Arcachon) showed higher respiration rates and metabolic adjustment to elevated temperatures; however, encapsulated embryos from the Solent showed no metabolic adjustment, high capsular mortalities and limited acclimation to high temperatures. Our results suggest that aerobic response of encapsulated embryos is locally adapted to the temperature history of their natal environment and illustrates the importance of local environmental history in determining the fate of key life stages in response to a changing marine climate.

The influence of ecological and life history factors on ectothermic temperature-size responses: Analysis of three Lycaenidae butterflies (Lepidoptera).

Body size has been shown to decrease with increasing temperature in many species, prompting the suggestion that it is a universal ecological response. However, species with complex life cycles, such as holometabolous insects, may have correspondingly complicated temperature-size responses. Recent research suggests that life history and ecological traits may be important for determining the direction and strength of temperature-size responses. Yet, these factors are rarely included in analyses. Here, we aim to determine whether the size of the bivoltine butterfly, Polyommatus bellargus, and the univoltine butterflies, Plebejus argus and Polyommatus coridon, change in response to temperature and whether these responses differ between the sexes, and for P. bellargus, between generations. Forewing length was measured using digital specimens from the Natural History Museum, London (NHM), from one locality in the UK per species. The data were initially compared to annual and seasonal temperature values, without consideration of life history factors. Sex and generation of the individuals and mean monthly temperatures, which cover the growing period for each species, were then included in analyses. When compared to annual or seasonal temperatures only, size was not related to temperature for P. bellargus and P. argus, but there was a negative relationship between size and temperature for P. coridon. When sex, generation, and monthly temperatures were included, male adult size decreased as temperature increased in the early larval stages, and increased as temperature increased during the late larval stages. Results were similar but less consistent for females, while second generation P. bellargus showed no temperature-size response. In P. coridon, size decreased as temperature increased during the pupal stage. These results highlight the importance of including life history factors, sex, and monthly temperature data when studying temperature-size responses for species with complex life cycles.

Historical shell size reduction of the dogwhelk (Nucella lapillus) across the southern UK.

Body size reduction is predicted to be one of the most common ecological responses to climate change, yet examples within some taxonomic groups, such as marine molluscs, are rare. Here, we document a significant reduction in shell size of the rocky shore gastropod Nucella lapillus across the southern UK using natural history collections and modern field data. These results are correlated with temporal changes in sea-surface temperature from a long-term monitoring station. The maximum height of N. lapillus shells has declined by approximately 18 mm over the past 100 years, and the median size of shells in large size classes declined by 6 mm during this time. Individuals are, on average, larger in the west than in the east, which is noted using both modern and historical samples. In some locations, there has been a local extinction of N. lapillus, potentially due to combined negative impacts of climate warming and TBT pollution. Our results further demonstrate the utility of natural history collections, paired with modern field sampling, to document biological response to climate change and other human impacts.

Historical and recent processes shaping the geographic range of a rocky intertidal gastropod: phylogeography, ecology, and habitat availability.

Factors shaping the geographic range of a species can be identified when phylogeographic patterns are combined with data on contemporary and historical geographic distribution, range-wide abundance, habitat/food availability, and through comparisons with codistributed taxa. Here, we evaluate range dynamism and phylogeography of the rocky intertidal gastropod Mexacanthina lugubris lugubris across its geographic range - the Pacific coast of the Baja peninsula and southern California. We sequenced mitochondrial DNA (CO1) from ten populations and compliment these data with museum records, habitat availability and range-wide field surveys of the distribution and abundance of M. l. lugubris and its primary prey (the barnacle Chthamalus fissus). The geographic range of M. l. lugubris can be characterized by three different events in its history: an old sundering in the mid-peninsular region of Baja (∼ 417,000 years ago) and more recent northern range expansion and southern range contraction. The mid-peninsular break is shared with many terrestrial and marine species, although M. l. lugubris represents the first mollusc to show it. This common break is often attributed to a hypothesized ancient seaway bisecting the peninsula, but for M. l. lugubris it may result from large habitat gaps in the southern clade. Northern clade populations, particularly near the historical northern limit (prior to the 1970s), have high local abundances and reside in a region with plentiful food and habitat - which makes its northern range conducive to expansion. The observed southern range contraction may result from the opposite scenario, with little food or habitat nearby. Our study highlights the importance of taking an integrative approach to understanding the processes that shape the geographic range of a species via combining range-wide phylogeography data with temporal geographic distributions and spatial patterns of habitat/food availability.

Ecological and evolutionary consequences of size-selective harvesting: how much do we know?

Size-selective harvesting, where the large individuals of a particular species are preferentially taken, is common in both marine and terrestrial habitats. Preferential removal of larger individuals of a species has been shown to have a negative effect on its demography, life history and ecology, and empirical studies are increasingly documenting such impacts. But determining whether the observed changes represent evolutionary response or phenotypic plasticity remains a challenge. In addition, the problem is not recognized in most management plans for fish and marine invertebrates that still mandate a minimum size restriction. We use examples from both aquatic and terrestrial habitats to illustrate some of the biological consequences of size-selective harvesting and discuss possible future directions of research as well as changes in management policy needed to mitigate its negative biological impacts.