graduate student, University of California, Santa Cruz
Examining why otters and related species are so species rich and diverse in body sizes and shapes
With 85 putative species and over 400 described extinct species, Musteloidea is a prime candidate to investigate patterns of adaptive radiation using both extant- and fossil-based macroevolutionary methods. The species diversity and equally impressive ecological and phenotypic disparity found across Musteloidea is often attributed to 2 adaptive radiations coinciding with 2 major climate events, the Eocene-Oligocene transition and the Mid-Miocene Climate Transition. Here, we compiled a novel time-scaled phylogeny for 88% of extant musteloids and used extant- and fossil-based phylogenetic methods to test predictions of adaptive radiation with respect to rates of lineage diversification and phenotypic evolution. Contrary to expectations, we found no evidence of an early burst in lineage diversification throughout the entire phylogeny, including during climatic transitions. Rather, we found strong support for decoupled diversification dynamics driven by increased clade carrying capacity in the branches leading to a subclade of elongate mustelids. Supporting decoupled diversification dynamics between the subclade of elongate mustelids and the ancestral musteloid regime is our finding of increased rates of body length evolution, but not body mass evolution, within the decoupled mustelid subclade. The discordance in evolutionary rates between body length and body mass along with evidence of decoupled diversification dynamics suggests that body elongation might be an innovation for the exploitation of novel Mid-Miocene resources, resulting in the diversification in some musteloids.
Abstract: Few species have been of more disputed affinities than the red or lesser panda (Ailurus fulgens), an endangered endemic Southeast Asian vegetarian member of the placental mammalian order Carnivora. This peculiar carnivoran has mostly been classified with raccoons (Procyonidae) or bears (Ursidae), grouped with the giant panda (Ailuropoda melanoleuca) in their own family, or considered a separate lineage of equivocal ancestry. Recent molecular studies have indicated a close affinity of the red panda to a clade of procyonids and mustelids (weasels, otters, martens, badgers, and allies), but have failed to unambiguously resolve the position of this species relative to mephitids (skunks and stink badgers). We examined the relationship of the red panda to other extant species of the carnivoran suborder Caniformia using a set of concatenated approximately 5.5-kb sequences from protein-coding exons of five nuclear genes. Bayesian, maximum likelihood, and parsimony phylogenetic analyses strongly supported the red panda as the closest living relative of a clade containing Procyonidae and Mustelidae to the exclusion of Mephitidae. These three families together with the red panda (which is classified here as a single extant species of a distinct family, Ailuridae) compose the superfamily Musteloidea, a clade strongly supported by all our phylogenetic analyses as sister to the monophyletic Pinnipedia (seals, sea lions, walruses). The approximately unbiased, Kishino-Hasegawa, and Templeton topology tests rejected (P<0.05) each of all possible alternative hypotheses about the relationships among the red panda and mephitids, procyonids, and mustelids. We also estimated divergence times for the red panda's lineage and ones of other caniform taxa, as well as the ages of the first appearance datums for the crown and total clades of musteloids and the total clades of the red panda, mephitids, procyonids, and mustelids. Bayesian relaxed molecular-clock analysis using combined information from all sampled genes yielded a approximately 42-Myr timescale to caniform evolution and provided evidence of five periods of increased diversification. The red panda's lineage and those of other extant musteloid families are estimated to have diverged during a 3-Myr interval from the mid-Early Oligocene to near the Early/Late Oligocene boundary. We present fossil evidence that extends the early adaptive radiation of the total clade of musteloids to the Eocene-Oligocene transition and also suggests Asia as a center of this radiation.
Pub.: 25 Aug '09, Pinned: 15 Jun '17
Abstract: We analyzed a concatenated (8492 bp) nuclear-mitochondrial DNA data set from 44 musteloids (including the first genetic data for Lyncodon patagonicus) with parsimony, maximum likelihood, and Bayesian methods of phylogenetic and biogeographic inference and two Bayesian methods of chronological inference. Here we show that Musteloidea emerged approximately 32.4-30.9 million years ago (MYA) in Asia, shortly after the greenhouse-icehouse global climate shift at the Eocene-Oligocene transition. During their Oligocene radiation, which proceeded wholly or mostly in Asia, musteloids diversified into four primary divisions: the Mephitidae lineage separated first, succeeded by Ailuridae and the divergence of the Procyonidae and Mustelidae lineages. Mustelidae arose approximately 16.1 MYA within the Mid-Miocene Climatic Optimum, and extensively diversified in the Miocene, mostly in Asia. The early offshoots of this radiation largely evolved into badger and marten ecological niches (Taxidiinae, Melinae, Mellivorinae, Guloninae, and Helictidinae), whereas the later divergences have adapted to other niches including those of weasels, polecats, minks, and otters (Mustelinae, Ictonychinae, and Lutrinae). Notably, and contrary to traditional beliefs, the morphological adaptations of badgers, martens, weasels, polecats, and minks each evolved independently more than once within Mustelidae. Ictonychinae (which is most closely related to Lutrinae) arose approximately 9.5-8.9 MYA, most likely in Asia, where it diverged into the Old World Ictonychini (Vormela, Poecilictis, Ictonyx, and Poecilogale) and New World Lyncodontini (Lyncodon and Galictis) lineages. Ictonychini presumably entered Africa during the Messinian Salinity Crisis (at the Miocene-Pliocene transition), which interposed the origins of this clade (approximately 6.5-6.0 MYA) and its African Poecilictis-Ictonyx-Poecilogale subclade (approximately 4.8-4.5 MYA). Lyncodontini originated approximately 2.9-2.6 MYA at the Pliocene-Pleistocene transition in South America, slightly after the emergence of the Panamanian land bridge that provided for the Great American Biotic Interchange. As the genera Martes and Ictonyx (as currently circumscribed) are paraphyletic with respect to the genera Gulo and Poecilogale, respectively, we propose that Pekaniaand Poecilictis be treated as valid genera and that "Martes"pennanti and "Ictonyx"libyca, respectively, be assigned to these genera.
Pub.: 14 Mar '12, Pinned: 15 Jun '17
Abstract: Rensch's rule states that sexual size dimorphism (SSD) increases with body size in taxa where males are larger, and decreases when females are larger. The dominant explanation for the trend is currently that competitive advantage for males is greater in larger individuals, whereas female size is constrained by the energetics of rearing offspring. This rule holds for a variety of vertebrate taxa, and opposing trends are rare. We examine the allometry of SSD within the Musteloidea and demonstrate a hypo-allometry contrary to Rensch's rule, with lower SSD associated with larger body size. We provide evidence that feeding ecology is involved. Where diet promotes group-living, the optimal strategy for the males of larger species is often not to attempt to defend access to multiple females, obviating any competitive advantage of relatively greater size. We conclude that the effect of feeding ecology on mating systems may be a hitherto neglected factor explaining variation in SSD.
Pub.: 01 Sep '16, Pinned: 15 Jun '17
Abstract: The niche divergence hypothesis suggests that if a species exhibits intersexual differences in diet, selection should favor divergence in the feeding apparatus between the sexes. Recent work revealed that male and female southern sea otters (Enhydra lutris nereis) utilize different dietary resources in response to increased population density; females exhibit more specialized diets as a function of smaller home ranges, whereas males exhibit larger home ranges, potentially allowing them to expand their dietary breadths by feeding on prey items that are not found in female home ranges. These dietary differences suggest the potential for sexual dimorphism of the feeding apparatus (i.e., the skull). Here, we tested the hypothesis that male and female southern sea otters exhibit differences in craniomandibular traits directly related to biting ability. Univariate and multivariate analyses of 12 craniomandibular traits showed that size is the primary axis of skull variation, whereas only a handful of craniomandibular traits demonstrated significant shape differences between the sexes. Relative postorbital constriction breadth, masseter in-lever length, and cranial height differed significantly between the sexes. These 3 traits can increase the surface area of jaw muscle attachment sites and thus are directly linked to the mechanics of biting ability. Collectively, these morphological differences indicate that niche divergence may be an important mechanism maintaining sexual dimorphism in southern sea otters.
Pub.: 06 Dec '16, Pinned: 12 Jun '17
Abstract: Adaptive radiation is hypothesized to be a primary mechanism that drives the remarkable species diversity and morphological disparity across the Tree of Life. Tests for adaptive radiation in extant taxa are traditionally estimated from calibrated molecular phylogenies with little input from extinct taxa. With 85 putative species in 33 genera and over 400 described extinct species, the carnivoran superfamily Musteloidea is a prime candidate to investigate patterns of adaptive radiation using both extant- and fossil-based macroevolutionary methods. The species diversity and equally impressive ecological and phenotypic diversity found across Musteloidea is often attributed to 2 adaptive radiations coinciding with 2 major climate events, the Eocene-Oligocene transition and the Mid-Miocene Climate Transition. Here, we compiled a novel time-scaled phylogeny for 88% of extant musteloids and used it as a framework for testing the predictions of adaptive radiation hypotheses with respect to rates of lineage diversification and phenotypic evolution. Contrary to expectations, we found no evidence for rapid bursts of lineage diversification at the origin of Musteloidea, and further analyses of lineage diversification rates using molecular and fossil-based methods did not find associations between rates of lineage diversification and the Eocene-Oligocene transition or Mid-Miocene Climate Transition as previously hypothesized. Rather, we found support for decoupled diversification dynamics driven by increased clade carrying capacity in the branches leading to a subclade of elongate mustelids. Supporting decoupled diversification dynamics between the subclade of elongate mustelids and the ancestral musteloid regime is our finding of increased rates of body length evolution, but not body mass evolution, within the decoupled mustelid subclade. The lack of correspondence in rates of body mass and length evolution suggest that phenotypic evolutionary rates under a single morphological metric, even one as influential as mass, may not capture the evolution of diversity in clades that exhibit elongate body shapes. The discordance in evolutionary rates between body length and body mass along with evidence of decoupled diversification dynamics suggests that body elongation might be an innovation for the exploitation of novel Mid-Miocene resources, resulting in the radiation of some musteloids.
Pub.: 05 May '17, Pinned: 12 Jun '17
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