Species-level heritability reaffirmed: a comment on "on the heritability of geographic range sizes"

For many current issues in macroevolution and macroecology, it is important to know to what degree the attributes of species are shared among closely related lineages, a concept sometimes referred to as species-level heritability. Recently, Webb and Gaston proposed a new method for analyzing the heritability of geographic range size and concluded that range size is not heritable in Cretaceous gastropods (data from Jablonski) and modern birds (their data). Here we show that Webb and Gaston's method is flawed in that it implicitly assumes that range sizes are uniformly distributed. When range size distributions show their characteristic strong right skew, Webb and Gaston's method spuriously tends to find that range sizes of closely related pairs of species are more dissimilar than the random expectation. A reanalysis of Jablonski's data finds range size to be robustly and strongly heritable in Cretaceous gastropods and less strongly but still significantly heritable in present-day birds.     

Range size heritability in Carnivora is driven by geographic constraints

Range size heritability refers to an intriguing pattern where closely related species occupy geographic ranges of similar extent. Its existence may indicate selection on traits emergent only at the species level, with interesting consequences for evolutionary processes. We explore whether range size heritability may be attributable to the fact that range size is largely driven by the size of geographic domains (i.e., continents, biomes, areas given by species' climatic tolerance) that tend to be similar in phylogenetically related species. Using a well-resolved phylogeny of Carnivora, we show that range sizes are indeed constrained by geographic domains and that the phylogenetic signal in range sizes diminishes if the domain sizes are accounted for. Moreover, more detailed delimitation of species' geographic domain leads to a weaker signal in range size heritability, indicating the importance of definition of the null model against which the pattern is tested. Our findings do not reject the hypothesis of range size heritability but rather unravel its underlying mechanisms. Additional analyses imply that evolutionary conservatism in niche breadth delimits the species' geographic domain, which in turn shapes the species' range size. Range size heritability patterns thus emerge as a consequence of this interplay between evolutionary and geographic constraints.     

On the heritability of geographic range sizes

Within taxonomic groups, most species are restricted in their geographic range sizes, with only a few being widespread. The possibility that species-level selection on range sizes contributes to the characteristic form of such species-range size distributions has previously been raised. This would require that closely related species have similar range sizes, an indication of "heritability" of range sizes at the species level. Support for this view came from a positive correlation between the range sizes of closely related pairs of fossil mollusc species. We extend this analysis by considering the relationship between the geographic range sizes of 103 pairs of contemporary avian sister species. Range sizes in these sister species show no evidence of being more similar to each other than expected by chance. A reassessment of the mollusc data also suggests that the high correlation was probably overestimated because of the skewed nature of range size data. The fact that sister species tend to have similar life histories and ecologies suggests that any relationship between range sizes and biology is likely to be complicated and will be influenced by historical factors, such as mode of speciation and postspeciation range size transformations.     

Mid-domain models as predictors of species diversity patterns: bathymetric diversity gradients in the deep sea

Geometric constraints represent a class of null models that describe how species diversity may vary between hard boundaries that limit geographic distributions. Recent studies have suggested that a number of large scale biogeographic patterns of diversity (e.g. latitude, altitude, depth) may reflect boundary constraints. However, few studies have rigorously tested the degree to which mid-domain null predictions match empirical patterns or how sensitive the null models are to various assumptions. We explore how variation in the assumptions of these models alter null depth ranges and consequently bathymetric variation in diversity, and test the extent to which bathymetric patterns of species diversity in deep sea gastropods, bivalves, and polychaetes match null predictions based on geometric constraints.
Range–size distributions and geographic patterns of diversity produced by these null models are sensitive to the relative position of the hard boundaries, the specific algorithms used to generate range sizes, and whether species are continuously or patchily distributed between range end points. How well empirical patterns support null expectations is highly dependent on these assumptions. Bathymetric patterns of species diversity for gastropods, bivalves and polychaetes differ substantially from null expectations suggesting that geometric constraints do not account for diversity–depth patterns in the deep sea benthos.     

Macroecology and the hierarchical expansion of evolutionary theory

The constraint envelope describing the relationship between geographical range size and body size has usually been explained by a minimum viable population size model, furnishing a strong argument for species selection if geographical range size turns out to be ‘heritable’. Recent papers have questioned this assumption of nonzero geographical range heritability at a phylogenetic level, meaning that the logic that constraint envelopes provide support for higher‐level selection fails. However, I believe that analysis of constraint envelopes can still furnish insights for the hierarchical expansion of evolutionary theory because the fitness furnished by variation in body size, which is frequently measured as a highly ‘heritable’ trait at the species level, can be partitioned into anagenetic and cladogenetic components. The constraint envelope furnishes an explicit mechanism for large‐body biased extinction rates influencing the distribution of body size. More importantly, it is possible to envisage a scenario in which anagenetic trends driving an increase in body size in higher latitudes within species (Bergmann's rule) are counteracted by available habitat area or continental edges constraining overall species distribution in these higher latitudes, increasing the probability of extinction. Under this combined model, faunas at higher latitudes and under habitat constraints may reach equilibrium points between these opposing hierarchical adaptive forces at smaller body size than faunas with less intense higher‐level constraints and will tend to be more right‐skewed.     

Evolution of the molluscan body plan: the case of the anterior adductor muscle of bivalves

The separated shell plates with the rearranged musculature (adductor muscle) is a novelty for bivalves. Despite its importance in the bivalve bodyplan, the development of the anterior adductor muscle remains unresolved. In this study, we investigate the myogenesis of the bivalve species Septifer virgatus to reveal the developmental origin of the larval muscles in bivalves, focusing on the anterior adductor muscle. We observed that larval retractor muscles are differentiated from the ectomesoderm in bivalves, and that the anterior adductor muscles are derived from primordial larval retractor muscles via segregation of the myoblast during the veliger larval stage. Through the comparative study of myogenesis in bivalves and its related taxa, gastropods, we found that both species possess myoblasts that emerge bilaterally and later meet dorsally. We hypothesize that these myoblasts, which are a major component of the main larval retractor in limpets, are homologous to the anterior adductor muscle in bivalves. These observations imply that the anterior adductor muscle of bivalves evolved as a novel muscle by modifying the attachment sites of an existing muscle.     

Heritability of brain size and surface features in rhesus macaques (Macaca mulatta)

The extent of heritability for overall brain size and regional cortical surface features such as sulcus lengths is important for demonstrating a genetic component to the observed phenotypic differences among individuals and for evaluating the potential for evolutionary change in response to selection. Although the genetics of brain size has been extensively considered, the detailed morphology of the cortical surface has not previously been subjected to genetic analysis. We estimated the heritability of brain size and cortical sulcus lengths using 438 endocranial casts taken from skeletons of rhesus macaques (Macaca mulatta) from the Cayo Santiago population. Estimates were obtained both by mother-offspring regression and symmetric-differences-squared (SDS) methods. Brain size, measured as cranial capacity, was highly and significantly heritable in this population, confirming results of previous studies with laboratory mice. Overall, cortical sulcus lengths were also heritable, with 35% of the sulci significantly heritable at the 5% level in the mother-offspring analysis. The average mother-offspring heritability estimate, 0.31, was the same as the average heritability obtained previously from a series of 56 cranial metric characters. The SDS analyses generally corresponded to the findings based on mother-offspring regressions, although the significance test appeared more conservative. Both gross and detailed morphology of the brain are heritable.     

Phylogenetic analyses of mode of larval development

Phylogenies based on morphological or molecular characters have been used to provide an evolutionary context for analysis of larval evolution. Studies of gastropods, bivalves, tunicates, sea stars, sea urchins, and polychaetes have revealed massive parallel evolution of similar larval forms. Some of these studies were designed to test, and have rejected, the species selection hypothesis for evolutionary trends in the frequency of derived larvae or life history traits. However, the lack of well supported models of larval character evolution leave some doubt about the quality of inferences of larval evolution from phylogenies of living taxa. Better models based on maximum likelihood methods and known prior probabilities of larval character state changes will improve our understanding of the history of larval evolution.     

THE HERITABLE BASIS OF VARIATION IN LARVAL DEVELOPMENTAL PATTERNS WITHIN POPULATIONS OF THE WOOD FROG (RANA SYLVATICA)

This study compares the heritable basis of variation in larval developmental patterns of mountain and lowland populations of the wood frog, Rana sylvatica. Additive genetic variances, heritabilities, and genetic correlations for larval developmental time and size at metamorphosis are estimated from half-sib and full-sib crosses. Considerable additive-genetic variances and high heritabilities are revealed for developmental time in both the mountain and the lowland population. There was a high level of additive-genetic variance and high heritability for body size at metamorphosis in the mountain population, but these were very low in the lowland population. The genetic correlations between developmental rate and larval body size are negative for the mountain population and near zero for the lowland population. It is argued that the differences in genetic structure between these two populations reflect differences in the selective regimes of their respective environments.     

Geographical range size heritability: what do neutral models with different modes of speciation predict?

Aim Phylogenetic conservatism or heritability of the geographical range sizes of species (i.e. the tendency for closely related species to share similar range sizes) has been predicted to occur because of the strong phylogenetic conservatism of niche traits. However, the extent of such heritability in range size is disputed and the role of biology in shaping this attribute remains unclear. Here, we investigate the level of heritability of geographical range sizes that is generated from neutral models assuming no biological differences between species. Methods We used three different neutral models, which differ in their speciation mode, to simulate the life‐history of 250,000 individuals in a square lattice of 50 × 50 cells. These individuals can speciate, reproduce, migrate and die in the metacommunity according to stochastic events. We ran each model for 3000 steps and recorded the range size of each species at each step. The heritability of geographical range size was assessed using an asymmetry coefficient between range sizes of sister species and using the coefficient of correlation between the range sizes of ancestors and their descendants. Results Our results demonstrated the ability of neutral models to mimic some important observed patterns in the heritability of geographical range size. Consistently, sister species exhibited higher asymmetry in range sizes than expected by chance, and correlations between the range sizes of ancestor–descendant species pairs, although often weak, were almost invariably positive. Main conclusions Our findings suggest that, even without any biological trait differences, statistically significant heritability in the geographical range sizes of species can be found. This heritability is weaker than that observed in some empirical studies, but suggests that even here a substantial component of heritability may not necessarily be associated with niche conservatism. We also conclude that both present‐day and fossil data sets may provide similar information on the heritability of the geographical range sizes of species, while the omission of rare species will tend to overestimate this heritability.     

Heritability, plasticity and canalization of Ural owl egg size in a cyclic environment

Avian egg size is highly variable on the population level, but is considered inflexible on the individual level. On the basis of 2969 measurements of individual eggs collected during 1981-2005, we analysed heritability, plasticity and selection on egg size in the Ural owl, a long-lived bird that preys on voles. Vole abundance varied in a 3-year cycle, creating varying food supply across the cycle's phases. Ural owl egg size is heritable (h(2) = 60%). Ural owls lay larger eggs in improved food conditions. On the basis of repeated breeding records of 59 females that bred in all vole cycle phases, we show that intra-individual adjustment (plasticity) explained 22.4% of the variation in egg size across phases. Egg size was under stabilizing selection. Extremely small and extremely large eggs had reduced hatchability, and individuals who laid either large or small eggs had lower lifetime fledgling production than the ones laying intermediately sized eggs. Our findings illustrate how maternal investment in egg size can both be heritable and highly responsive to variable environmental conditions, and suggest that variation in the investment in egg size across individuals is canalized.     

Early Shell Formation During Molluscan Embryogenesis, with New Studies on the Surf Clam, Spisula solidissima

Shell formation in molluscs begins early in embryogenesis duringsome stage of archenteron formation. Ultrastructural informationon early formation of external shells is available from onlya few bivalves and gastropods. Secretion of the very first shellmaterial by shell field epithelial cells is preceded by an invaginationof the dorsal ectoderm in the region of the shell field. A centuryago, this invagination was termed the "shell gland." As a secretoryfunction for this invagination has not yet been demonstratedand as the term "shell gland" has taken on various meaningsin the literature, the invagination will be referred to as theshell field invagination. The opening into the shell field invaginationseems to be circular in gastropods and elongate in bivalves.Accordingly initial organic shell material seems to form a ringin gastropods and a saddle in bivalves. As in adult molluscs,shells of pre-metamorphic molluscs are composed of both organicand inorganiccomponents. Ultrastructural data from bivalvesand gastropods indicate that the initial organic shell materialis secreted just outside the shell field invagination (acrossthe pore). Initial inorganic shell materials have not been localizednor their pathway traced into or through any pre-metamorphicmolluscs. New SEM and TEM data show that the invagination inthe bivalve Spisula solidissima is composed of a wide outerregion and very narrow inner region with the first shell materialforming at the junction between the two. This is unlike ultrastructuraldata available for other species. Many sections give the falseimpressions that: 1) the shell field invagination is closedto the outside and, 2) that the first organic shell materiallines the innermost region of the invagination. It is not clearwhether the cells of the outer invagination in this speciesare shell field cells. It is suggested that they are not.     

The relationship between geographic range size and life history traits: is biogeographic history uncovered? A test using the Iberian butterflies

The geographic range of a species is influenced by past phylogenetic and biogeographic patterns. However, other historical interactions, including the interplay between life history and geography, are also likely involved. Therefore, the range size of a species can be explained on the basis of niche‐breadth or dispersal related hypotheses, and previous work on European butterflies suggests that both, under the respective guise of ecological specialisation and colonising ability may apply. In the present study, data from 205 species of butterflies from the Iberian peninsula were processed through multiple regression analyses to test for correlations between geographic range size, life history traits and geographic features of the species distribution types. In addition, the percentage of variance explained by the subsets of variables analyzed in the study, with and without control for phylogenetic effects was tested. Despite a complex pattern of bivariate correlations, we found that larval polyphagy was the single best correlate of range size, followed by dispersal. Models that combined both life history traits and geographic characteristics performed better than models generated independently. The combined variables explained at least 39% of the variance. Bivariate correlations between range size and body size, migratory habits or egg size primarily reflected taxonomic patterning and reciprocal correlations with larval diet breadth and adult phenology. Therefore, aspects of niche breadth i.e. potential larval diet breadth emerged as the most influential determinants of range size. However, the relationships between these types of ecological traits and biogeographic history must still be considered when associations between life history and range size are of interest.     

Larval ecology and morphology in fossil gastropods

The shell of marine gastropods conserves and reflects early ontogeny, including embryonic and larval stages, to a high degree when compared with other marine invertebrates. Planktotrophic larval development is indicated by a small embryonic shell (size is also related to systematic placement) with little yolk followed by a multiwhorled shell formed by a free‐swimming veliger larva. Basal gastropod clades (e.g. Vetigastropoda) lack planktotrophic larval development. The great majority of Late Palaeozoic and Mesozoic ‘derived’ marine gastropods (Neritimorpha, Caenogastropoda and Heterobranchia) with known protoconch had planktotrophic larval development. Dimensions of internal moulds of protoconchs suggest that planktotrophic larval development was largely absent in the Cambrian and evolved at the Cambrian–Ordovician transition, mainly due to increasing benthic predation. The evolution of planktotrophic larval development offered advantages and opportunities such as more effective dispersal, enhanced gene flow between populations and prevention of inbreeding. Early gastropod larval shells were openly coiled and weakly sculptured. During the Mid‐ and Late Palaeozoic, modern tightly coiled larval shells (commonly with strong sculpture) evolved due to increasing predation pressure in the plankton. The presence of numerous Late Palaeozoic and Triassic gastropod species with planktotrophic larval development suggests sufficient primary production although direct evidence for phytoplankton is scarce in this period. Contrary to previous suggestions, it seems unlikely that the end‐Permian mass extinction selected against species with planktotrophic larval development. The molluscan classes with highest species diversity (Gastropoda and Bivalvia) are those which may have planktotrophic larval development. Extremely high diversity in such groups as Caenogastropoda or eulamellibranch bivalves is the result of high phylogenetic activity and is associated with the presence of planktotrophic veliger larvae in many members of these groups, although causality has not been shown yet. A new gastropod species and genus, Anachronistella peterwagneri, is described from the Late Triassic Cassian Formation; it is the first known Triassic gastropod with an openly coiled larval shell.     

Gastropods and bivalves taken as by-catch in the deep-water shrimp trawl-fishery along the Pacific coast of Costa Rica,Central America

Deep-water habitats are among the least studied but most vulnerable environments. By-catch data from deep-water fisheries in Latin America are limited, and detailed reports on associated molluscs are scarce. This study provides information on deep-water shelled molluscs collected between 2010 and 2011 by commercial shrimp trawling fisheries along the Pacific coast of Costa Rica at depths from 112 to 271?m. Twenty-six species were identified, 23 gastropods and three bivalves. Our data extend the depth range of 14 species, and Homalopoma cf. grippii is reported for the first time for Costa Rica. The most common species were the gastropods Fusinus spectrum, Polystira nobilis and Solenosteira gatesi. Only one species (Sinum debile) was captured below 250?m. The catch of molluscs per unit effort was influenced by depth, but not by seasonality or geographic area. It is speculated that these long-lasting bottom-trawling activities have caused negative effects on species diversity and mollusc biomass. Nevertheless, a monitoring program is recommended to assess possible impacts of this type of fishery on mollusc diversity and biomass.     

BATHYMETRIC PATTERNS OF BODY SIZE IN DEEP-SEA GASTROPODS

The shift to smaller body size in marine invertebrates at the deep-sea threshold and size-depth clines within the deep-sea ecosystem are global biogeographic phenomena that remain poorly understood. We present the first standardized measurements of larval and adult size among ecologically and phylogenetically similar species across a broad and continuous depth range, using the largest family of deep-sea gastropods (the Turridae). Size at all life stages increases significantly with depth from the upper bathyal region to the abyssal plain. These consistent clines may result from selection favoring larger size at greater depths because of its metabolic and competitive advantages. The unusually small size of deep-sea mollusks, in general, may represent an independent evolutionary process that favors invasion by inshore taxa composed of small organisms.     

Null models of geographic range size evolution reaffirm its heritability

Most models of allopatric speciation predict that the two daughter species will have range sizes different from each other's and potentially from that of their common ancestor. However, I find that this difference is less than that expected under a variety of null models of range evolution. Sister species' range values may therefore become more similar in the time following speciation. Greater-than-expected similarity (symmetry) has also been treated as a form of range size heritability. I therefore compare the results of this symmetry approach to a test for phylogenetic signal, using the range sizes of North American birds. I find that range size is heritable under both tests. I suggest that null models for range size heritability should be informed by an explicit model of evolution. Comparative methods may give erroneous results if they fail to take the unusual form of inheritance of range size into account.     

Genetic polymorphism and trade-offs in the early life-history strategy of the Pacific oyster, Crassostrea gigas (Thunberg, 1795): a quantitative genetic study

We investigated genetic variability and genetic correlations in early life-history traits of Crassostrea gigas. Larval survival, larval development rate, size at settlement and metamorphosis success were found to be substantially heritable, whereas larval growth rate and juvenile traits were not. We identified a strong positive genetic correlation between larval development rate and size at settlement, and argue that selection could optimize both age and size at settlement. However, trade-offs, resulting in costs of metamorphosing early and large, were suggested by negative genetic correlations or covariances between larval development rate/size at settlement and both metamorphosis success and juvenile survival. Moreover, size advantage at settlement disappeared with time during the juvenile stage. Finally, we observed no genetic correlations between larval and juvenile stages, implying genetic independence of life-history traits between life-stages. We suggest two possible scenarios for the maintenance of genetic polymorphism in the early life-history strategy of C. gigas.     

Dissecting latitudinal diversity gradients: functional groups and clades of marine bivalves

The latitudinal diversity gradient, with maximum taxonomic richness in the tropics, is widely accepted as being pervasive on land, but the existence of this pattern in the sea has been surprisingly controversial. This is partly due to Thorson's influential claim that the normal latitudinal diversity gradient occurs in marine epifauna (taxa living on the surface of the substratum) but not in infauna (burrowing or boring into the substratum), a contrast he attributed to the greater spatial and temporal environmental homogeneity of infaunal habitats. In an analysis of 930 species of north-eastern Pacific marine shelf bivalves, we found that bivalves as a whole, and both infauna and epifauna separately, show a strong latitudinal diversity gradient (measured as number of species per degree latitude) that is closely related to mean sea surface temperature (SST), even in analyses of residuals and first differences. This agrees with results for marine gastropods, but contradicts Thorson's environmental homogeneity hypothesis. The relationship between SST and diversity is consistent with a species-energy hypothesis, but the linkages from SST to diversity remain unclear. Most bivalve clades within broad functional groups conform to the general latitudinal trend, except for the deposit-feeding protobranchs. This group's non-directional pattern may be related to its mode of development, because a similar effect is seen in several other groups locked into this low-fecundity, non-feeding larval mode.