Sympatric speciation by allochrony?

Sympatric speciation was once thought most improbable, but careful study of some systems, particularly the apple maggot (Rhagoletis pomonella) and related Rhagoletis species, has led to its reinstatement as a likely mode of speciation in some cases. Different species and host races in this clade of flies often have highly specialized host preference, and along with frequent evolutionary shifts to different fruit species between sister taxa, there is a likely effect of the timing of adult emergence that follows host fruiting phenology. This is known as “allochronic” isolation (from the Greek meaning “different timing”). This overview covers recent discoveries by Inskeep et al. (Molecular Ecology, 2021) showing how allochrony is a major factor in preventing gene flow between a pair of sister species of Rhagoletis on different host fruits. Although the authors do not claim to prove sympatric speciation, it does seem very likely, and the work clearly underscores how readily host shifts via allochrony can aid sympatric speciation

Who wins when the competition heats up? Effects of climate change on interactions among three Antarctic penguin species

This thesis sought to elucidate the mechanisms driving the large-scale population changes observed in Pygoscelis penguins in the Western Antarctic Peninsula (WAP)/Scotia Sea region since the 1970s, with particular focus on the interactions between the species. During this period the climate in this region has changed dramatically, with rapid warming and sea ice declines occurring until the late 20th century to be followed by a pause in the warming. These changes have altered biotic and abiotic conditions in the penguins’ ecosystem and researchers widely agree that this is driving their population changes. In order to elucidate the exact mechanisms of population change, we attempted to fill crucial knowledge gaps, including foraging ecology, migration and breeding success, throughout their annual cycle and all with particular focus on the interactions between the three Pygoscelis species. Direct tracking and isotope analysis provided novel insights into foraging behaviour and the role of niche partitioning between the species throughout the annual cycle, and its importance for reducing interspecific competition. During the breeding season, allochrony between Adélie and chinstrap penguins was found to reduce competitive overlap in foraging areas by 54%, compared to synchronous breeding, and to be resilient to climate change. The migration routes and over-winter sites of chinstrap penguins from the South Orkney Islands were identified for the first time and were found to be segregated from birds from the neighbouring South Shetland Islands archipelago. The environmental conditions at the two over-winter sites differed but the population trends at the two archipelagos were similar, suggesting that winter conditions are not likely to be a major driver. Developing on our findings of contrasting environmental conditions across the chinstrap over-wintering sites, we investigated the effect of multiple environmental variables on population trends in the final two thesis chapters. Sea ice has been shown to be a major driver of Adélie penguin breeding success, and thereby population trends, and birds in our study region experience particularly dramatic seasonal changes in sea ice concentration (SIC), as it is located near the northern extent of winter ice. The three Pygoscelis species are widely cited as having different ice tolerances, termed the ‘sea ice hypothesis’, with Adélies being described as ‘ice-loving’, chinstraps as ‘ice tolerant’ and gentoos as ‘ice averse’. These differing ice tolerances are thought to be a major factor in the species’ contrasting population changes in this region and these hypothesised preferences could theoretically induce a sea ice optima for breeding and forging success. However, no evidence was found for a sea ice optima at the study colony, despite previous studies finding a 20% optima for Adélies in East Antarctica, and SIC was found to have no significant effect on breeding productivity or diet composition but some effect was found for fledging mass and foraging trip duration. The combined influence of environmental conditions and interspecific interactions on the three species’ population trends was investigated for the first time in this system. Data from large and local scale climate and a long time period (more than 25 years) were investigated at the two study archipelagos using a multi-species Gompertz population model. The model failed to identify any of the modelled variables as major drivers of the population variation, suggesting that other factors, such as predation and prey availability were potentially important drivers. This thesis also identified a number of priorities for future research and identified the need for a greater emphasis on modelling the effects of Antarctic krill biomass, rather than climate variables, upon penguin demographic variables

Influence of climate and fisheries on the demography of giant petrels

ThesisUnderstanding how populations and communities will respond to global changes is a major focus of modern ecology, and demographic studies are crucial for understanding the dynamic of wild populations and their responses to change. Here, I first conducted an analytically robust literature to demonstrate that seabird mortality in global fisheries (bycatch) tends to be biased by sex and age, mainly related to differential at-sea distributions, underpinning the population level effect bycatch on the most threatened group of birds. Next I performed a comprehensive longitudinal study, to address effects of fisheries, environmental variability and climate oscillation on population dynamics of northern (NGP, Macronectes halli) and southern giant petrel (SGP, M. giganteus) at Bird Island, South Georgia. I showed that annual survival and breeding success of NGP and SGP was influenced mainly by climatic oscillation and oceanographic conditions, including fisheries, and that the responses varied by sex and age. Giant petrels survived and reproduced better in warmer years, contrasting with the negative effects of warmer conditions on a range of marine land-based vertebrates in the same ecosystem. Differential accessibility to food resources during chick-rearing due to allochrony have contributed for the NGP breeding success and delayed reproductive senescence compared to SGP, supporting empirical evidence for role of allochrony on their divergent population trajectories. Finally, the findings in this thesis sheds a new light on how phenological mismatch can influence demographic process and on the role of environmental conditions on reproductive senescence, which are among the poorest understood processes in population ecology.Science Without Borders Program (CNPq/Brazil

Niche partitioning of sympatric penguins by leapfrog foraging is resilient to climate change

1.Interspecific competition can drive niche partitioning along multidimensional axes, including allochrony. Competitor matching will arise where the phenology of sympatric species with similar ecological requirements respond to climate change at different rates such that allochrony is reduced. 2.Our study quantifies the degree of niche segregation in foraging areas and depths that arises from allochrony in sympatric Adélie and chinstrap penguins and explores its resilience to climate change. 3.Three‐dimensional tracking data were sampled during all stages of the breeding season and were used to parameterise a behaviour‐based model that quantified spatial overlap of foraging areas under different scenarios of allochrony. 4.The foraging ranges of the two species were similar within breeding stages, but differences in their foraging ranges between stages, combined with the observed allochrony of 28 days, resulted in them leapfrogging each other through the breeding season such that they were exploiting different foraging locations on the same calendar dates. Allochrony reduced spatial overlap in the peripheral utilisation distribution of the two species by 54.0% over the entire breeding season, compared to a scenario where the two species bred synchronously. 5.Analysis of long‐term phenology data revealed that both species advanced their laying dates in relation to October air temperatures at the same rate, preserving allochrony and niche partitioning. However if allochrony is reduced by just a single day, the spatial overlap of the core utilisation distribution increased by an average of 2.1% over the entire breeding season. 6.Niche partitioning between the two species by allochrony appears to be resilient to climate change and so competitor matching cannot be implicated in the observed population declines of the two penguin species across the Western Antarctic Peninsula

The role of allochrony in influencing interspecific differences in foraging distribution during the non-breeding season between two congeneric crested penguin species

Mechanisms promoting coexistence between closely related species are fundamental for maintaining species diversity. Mechanisms of niche differentiation include allochrony which offsets the peak timing of resource utilisation between species. Many studies focus on spatial and temporal niche partitioning during the breeding season, few have investigated the role allochrony plays in influencing interspecific segregation of foraging distribution and ecology between congeneric species during the non-breeding season. We investigated the non-breeding migrations of Snares (Eudyptes robustus) and Fiordland penguins (Eudyptes pachyrhynchus), closely related species breeding between 100–350 km apart whose migration phenology differs by two months. Using light geolocation tracking, we examined the degree of overlap given the observed allochrony and a hypothetical scenario where the species commence migration simultaneously. We found that Fiordland penguins migrated to the Sub-Antarctic Frontal Zone and Polar Frontal Zone in the austral autumn whereas Snares penguins disperse westwards staying north of the Sub-Tropical Front in the austral winter. Our results suggest that allochrony is likely to be at the root of segregation because the relative profitability of the different water masses that the penguins forage in changes seasonally which results in the two species utilising different areas over their core non-breeding periods. Furthermore, allochrony reduces relatively higher levels of spatiotemporal overlap during the departure and arrival periods, when the close proximity of the two species’ colonies would cause the birds to congregate in similar areas, resulting in high interspecific competition just before the breeding season. Available evidence from other studies suggests that the shift in phenology between these species has arisen from adaptive radiation and phenological matching to the seasonality of local resource availability during the breeding season and reduced competitive overlap over the non-breeding season is likely to be an incidental outcome

Cryptic species and independent origins of allochronic populations within a seabird species complex (Hydrobates spp.)

Humans are inherently biased towards naming species based on morphological differences, which can lead to reproductively isolated species being mistakenly classified as one if they are morphologically similar. Recognising cryptic diversity is needed to understand drivers of speciation fully, and for accurate estimates of global biodiversity and assessments for conservation. We investigated cryptic species across the range of band-rumped storm-petrels (Hydrobates spp.): highly pelagic, nocturnal seabirds that breed on tropical and sub-tropical islands in the Atlantic and Pacific Oceans. In many breeding colonies, band-rumped storm-petrels have sympatric but temporally isolated (allochronic) populations; we sampled all breeding locations and allochronic populations. Using mitochondrial control region sequences from 754 birds, cytochrome b sequences from 69 birds, and reduced representation sequencing of the nuclear genomes of 133 birds, we uncovered high levels of genetic structuring. Population genomic analyses revealed up to seven unique clusters, and phylogenomic reconstruction showed that these represent seven monophyletic groups. We uncovered up to six independent breeding season switches across the phylogeny, spanning the continuum from genetically undifferentiated temporal populations to full allochronic species. Thus, band-rumped storm-petrels encompass multiple cryptic species, with non-geographic barriers potentially comprising strong barriers to gene flow

Ecological Factors Explaining Genetic Differentiation in Aphidomorpha Associated with Pecan and Water Hickory Trees

Host-associated differentiation (HAD) is a form of ecologically mediated host-race formation between parasite populations. Since HAD can ultimately lead to speciation, it has been proposed as a way to account for the vast species diversity observed in parasitic arthropods. However, the importance of HAD to species diversity is unclear because the factors explaining the occurrence of HAD are only partially understood. Still, there are several examples of parasite-host case study systems for which there is a known cause of reproductive isolation between host-associated parasite populations. Thus, several biological and ecological factors (e.g., immigrant inviability or allochrony) have been proposed as explanatory factors for HAD occurrence. The body of research presented here represents the first quantitative assessment of the generalized relationship between HAD occurrence and the incidence of the proposed explanatory factors. This research was supported by field experiments that assessed the co-occurrence of HAD and particularly important explanatory factors. These experiments were conducted in a community of Aphidomorpha species living on pecan and water hickory trees. I found that HAD can be explained in general based on the incidence of specific explanatory factors (i.e. immigrant inviability, gall-making, short generation times, volatile preference, morphological differentiation, and host-shifting opportunities). These factors were used to create a hierarchy of conditional probabilities that can successfully separate the presence of HAD from its absence. The field experiments corroborated that the occurrence of HAD is correlated with immigrant inviability as well as allochrony

Genetic and ecological consequences of a shifted phenology in a forest defoliator

Doutoramento em Engenharia Florestal e dos Recursos Naturais - Instituto Superior de AgronomiaThaumetopoea pityocampa is a major pine defoliatior over the Mediterranean Basin. An atypical population with a shifted phenology, ongoing an allochronic differentiation process, was recently discovered in Mata Nacional Leiria, Portugal. The shifted population reproduces in spring achieving its larval development during summer (SP), whereas the sympatric typical population reproduces in summer and has winter larval development (WP). They are reproductively isolated through time, although sharing the same space and host species. General objectives of this work were to characterize the current and potential distribution range of this population, its spatial/temporal genetic and demographic patterns, and ecological adaptations. Field monitoring of presence/absence of SP nests throughout Leiria showed that it is expanding to North and South. Current distribution is restricted to coastal areas, along ca. 120 x 20 km area. Distribution models predict that its distribution will be restricted to coastal areas, due to unsuitable climate inland, being the maximal temperatures of the summer months the main constraint. A phylogeographic study confirmed high SP differentiation from other Portuguese populations. A spatio-temporal sampling along two geographic transects in Leiria zone revealed high stability in time of the genetic composition and structure. A striking demographic result showed that SP tends to apparently displace the WP from the coastal zones suggesting a possible competition phenomenon. Gene flow between the two populations was shown to remain low, even if some SP males actually emerge late. Ecological differentiation was assessed at egg and larval stages. The effect of a wide range of high temperatures on egg survival and development showed higher performances of the SP. Furthermore, SP larvae showed a better ability to cope with host plant water stress, evidencing adaptation to summer feeding activity. This study highlights intra-specific variations on the response of this insect to environmental constraints evidencing ecological adaptation following allochronic differentiationN/

Species-specific pace of development is associated with differences in protein stability

Although many molecular mechanisms controlling developmental processes are evolutionarily conserved, the speed at which the embryo develops can vary substantially between species. For example, the same genetic program, comprising sequential changes in transcriptional states, governs the differentiation of motor neurons in mouse and human, but the tempo at which it operates differs between species. Using in vitro directed differentiation of embryonic stem cells to motor neurons, we show that the program runs more than twice as fast in mouse as in human. This is not due to differences in signaling, nor the genomic sequence of genes or their regulatory elements. Instead, there is an approximately two-fold increase in protein stability and cell cycle duration in human cells compared with mouse cells. This can account for the slower pace of human development and suggests that differences in protein turnover play a role in interspecies differences in developmental tempo