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Evolutionary shifts in extant mustelid (Mustelidae: Carnivora) cranial shape, body size and body shape coincide with the Mid-Miocene Climate Transition

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Biology Letters
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Chris J Law at University of Washington
Chris J Law
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Abstract

Environmental changes can lead to evolutionary shifts in phenotypic traits, which in turn facilitate the exploitation of novel adaptive landscapes and lineage diversification. The global cooling, increased aridity and expansion of open grasslands during the past 50 Myr are prime examples of new adaptive landscapes that spurred lineage and ecomorphological diversity of several mammalian lineages such as rodents and large herbivorous megafauna. However, whether these environmental changes facilitated evolutionary shifts in small- to mid-sized predator morphology is unknown. Here, I used a complete cranial and body morphological dataset to examine the timing of evolutionary shifts in cranial shape, body size and body shape within extant mustelids (martens, otters, polecats and weasels) during the climatic and environmental changes of the Cenozoic. I found that evolutionary shifts in all three traits occurred within extant mustelid subclades just after the onset of the Mid-Miocene Climate Transition. These mustelid subclades first shifted towards more elongate body plans followed by concurrent shifts towards smaller body sizes and more robust crania. I hypothesize that these cranial and body morphological shifts enabled mustelids to exploit novel adaptive zones associated with the climatic and environmental changes of the Mid to Late Miocene, which facilitated significant increases in clade carrying capacity.
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Research
Cite this article: Law CJ. 2019 Evolutionary
shifts in extant mustelid (Mustelidae:
Carnivora) cranial shape, body size and body
shape coincide with the Mid-Miocene Climate
Transition. Biol. Lett. 15: 20190155.
http://dx.doi.org/10.1098/rsbl.2019.0155
Received: 1 March 2019
Accepted: 8 May 2019
Subject Areas:
evolution
Keywords:
body elongation, diversification, ecological
opportunity, morphological innovation,
Musteloidea, trait evolution
Author for correspondence:
Chris J. Law
e-mail: cjlaw@ucsc.edu
Electronic supplementary material is available
online at https://dx.doi.org/10.6084/m9.
figshare.c.4507244.
Evolutionary biology
Evolutionary shifts in extant mustelid
(Mustelidae: Carnivora) cranial shape,
body size and body shape coincide with
the Mid-Miocene Climate Transition
Chris J. Law
Ecology and Evolutionary Biology, University of California Santa Cruz, 130 McAllister Way, Santa Cruz,
CA 95060, USA
CJL, 0000-0003-1575-7746
Environmental changes can lead to evolutionary shifts in phenotypic traits,
which in turn facilitate the exploitation of novel adaptive landscapes and
lineage diversification. The global cooling, increased aridity and expansion
of open grasslands during the past 50 Myr are prime examples of new
adaptive landscapes that spurred lineage and ecomorphological diversity
of several mammalian lineages such as rodents and large herbivorous
megafauna. However, whether these environmental changes facilitated
evolutionary shifts in small- to mid-sized predator morphology is unknown.
Here, I used a complete cranial and body morphological dataset to examine
the timing of evolutionary shifts in cranial shape, body size and body shape
within extant mustelids (martens, otters, polecats and weasels) during the
climatic and environmental changes of the Cenozoic. I found that evolution-
ary shifts in all three traits occurred within extant mustelid subclades just
after the onset of the Mid-Miocene Climate Transition. These mustelid
subclades first shifted towards more elongate body plans followed by
concurrent shifts towards smaller body sizes and more robust crania.
I hypothesize that these cranial and body morphological shifts enabled
mustelids to exploit novel adaptive zones associated with the climatic and
environmental changes of the Mid to Late Miocene, which facilitated
significant increases in clade carrying capacity.
1. Introduction
The exceptional lineage and phenotypic diversity found across the tree of life is
often associated with increases in ecological opportunities through the evolution
of innovations, extinction of competitors or environmental changes [1– 3]. Simpson
[1] was one of the first to recognize that the adaptive landscapes of phenotypic traits
can shift ( jump) in response to environmental changes. The global cooling,
increased aridity and habitat shift from forest to grasslands during the past
50 Myr [4– 7] is a prime exampleofenvironmental changes that spurred evolution-
ary shifts in phenotypes. Several mammalian clades have adapted to these
environmental transitions towards more open, grass-dominated habitats. Rodents
and lagomorphs diversified and shifted towards increased tooth crown height
(i.e. hypsodonty) to eat tougher grass material and evolved adaptations for more
efficient burrowing, jumping and cursorial locomotion across the open habitats
(reviewed in [8]). Herbivorous ungulates also shifted towards hypsodont dentition
during the Oligocene to Miocene, along with the lengthening of limbs for more effi-
cient cursoriality during the late Miocene [9–12]. Similarly, ecomorphological
diversity of carnivores increased [13–15], with large carnivores shifting from
ambush specialists to active pursuit specialists during the late Miocene to
&2019 The Author(s) Published by the Royal Society. All rights reserved.
... mya, Gibbard & Head, 2020) represents a time of taxonomic stasis at the species level but immense intraspecific variation. The species' originations are related to ecological impact through climate change in the Late Miocene and Pliocene (Edwards et al., 2010;King, 1989;Koepfli et al., 2008;Law, 2019;Law et al., 2018;Strömberg, 2011). The diversification and expansion of small mustelids in the northern hemisphere during the Pliocene, especially of Meles Linnaeus, 1758, Martes Pinel, 1792, and Mustela Linnaeus, 1758, made Mustelidae especially successful among Carnivora of the time. ...
... The diversification and expansion of small mustelids in the northern hemisphere during the Pliocene, especially of Meles Linnaeus, 1758, Martes Pinel, 1792, and Mustela Linnaeus, 1758, made Mustelidae especially successful among Carnivora of the time. These extraordinary evolutionary abilities characterize mustelid representatives up to today (Law, 2019;Law et al., 2018;Liu et al., 2023). ...
... Mustelids are particularly useful for biochronological correlations of the Pleistocene. Their remains often occur in large numbers, are widespread encompassing most of the Holarctic, and underwent rapid evolutionary changes in morphology (Edwards et al., 2010;King, 1989;Koepfli et al., 2008;Law, 2019;Law et al., 2018Law et al., , 2019Strömberg, 2011). Among the main characters that distinguish evolutionary stages within mustelids, the transversal Abbreviations: B, buccolingual breadth; Ba, mesial breadth; Bp, distal breadth; B ta, talonid breadth; B tr, trigon(id) breadth; dB, dorsomedial diameter of the distal epiphysis; dL, caudomedial diameter of the distal epiphysis; L, mesio-distal length; L ta, talon(id) length; L tr, trigon (id) length; M, mean; mc, metacarpal; mB, dorsomedial diameter of the shaft; mL, caudomedial diameter of the shaft; mm, millimeter; MNI, minimum number of individuals; mt, metatarsal; N, number in the sample; NISP, number of identified specimens; pB, dorsomedial diameter of the proximal epiphysis; pL, caudomedial diameter of the proximal epiphysis. ...
Importance of the mustelids from the Early Pleistocene site Schernfeld (Bavaria, Germany) on the Eurasian context
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The Early Pleistocene fossil site of Schernfeld, a karst fissure filled with an ossiferous breccia, is well known due to the abundant fossil remains, mainly of micromammals and carnivores. Since the discovery, the taxonomic status of the Schernfeld mustelids has caused controversy and, consequently, various authors have listed different species. Until recently, none of these species has been the subject of adequate studies. A detailed revision of the Schernfeld mustelids material was made through comparative morphology based on mustelids from other European Early and early Middle Pleistocene sites. It reveals the presence of five mustelids: Gulo gulo schlosseri, Martes vetus, Meles meles, Mustela palerminea, and Mustela praenivalis. Their remains are characterized by ancestral features, especially in M. vetus, M. palerminea, and M. praenivalis. Due to the morphology of mustelids and the taxonomical composition of the Schernfeld fauna, the biochronological age of the entire assemblage was re‐evaluated and assessed for ca. 1.9–1.7 mya.
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... Myr (Patterson et al., 2021). Previously, most species were determined as Mustela (Koepfli et al., 2008;Law et al., 2018;Law, 2019). Additionally, data inferred from mitochondrial genomes showed that the genus Mustela already had appeared 11.8-10.3 ...
... In the evolution of the Mustelidae, one of the most crucial periods is the Mid-Miocene Climate Transition (MMCO, 16.1-11.6 Myr; Edwards et al., 2010;Strömberg, 2011;Law, 2019). The period was characterised by massive expansion of the Antarctic ice sheet and global cooling, which resulted in an increase of grasslands (Flower and Kennett, 1994;Böhme, 2003;Doláková et al., 2020). ...
... Associated with it, the diversification of rodents and lagomorphs during that period led to increases in many clades among the mustelids, particularly forms like the Mustelinae (Finarelli and Badgley, 2010;Fabre et al., 2012;Samuels and Hopkins, 2017). The carrying capacity of various mustelines for those environmental changes involved decreases in size and shifts towards small, elongate bodies (King, 1989;Koepfli et al., 2008;Edwards et al., 2010;Strömberg, 2011;Law et al., 2018;Law, 2019). Evolutionary plans during that time may have facilitated diversification by allowing mustelids to chase prey in tight burrows and tunnels and small crevices (Law et al., 2018;Law, 2019;Liu et al., 2023). ...
Baranogale helbingi Kormos, 1934 (Mustelidae, Carnivora) from the late Pliocene site Węże 1 (Poland)
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The ancient and archaic mustelid Baranogale helbingi is a European endemit. Its occurrence is characteristic for the Pliocene, but the species occurred also during the early Pleistocene. Among 30 sites, where its occurrence is documented, 8 are located in Poland. Among them, the most abundant material was found at Węże 1, dated at 3.6–3.2 Myr. The newly described remains, with two relatively well preserved skulls, broadly expand knowledge about the species. Morphometrical analysis showed the important role of sexual dimorphism in the variability of the species. Like other European Ictonychini, B. helbingi vanished during the early Pleistocene, owing to competition with small Mustelinae that were extremely adaptable in terms of ecology.
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... Therefore, we observed larger individuals in the water that most likely overcame the physiological restrictions imposed by this habitat, in spite of their exclusively carnivorous habit (Fig. 3d). Despite body size of predators and prey being positively correlated in some groups (Shine, 1991;Portalier et al., 2018), a previous study revealed that abiotic constraints were crucial on evolutionary shifts in mustelids body plan (Law, 2019), that allowed them to explore new environments for resources (see below; King & Powell, 2006). One of these modifications was the broader cranial shape and large jaw muscles, which compensate for their small bodies allowing them to consume prey up to 10 times larger than their own body mass (Law, 2019). ...
... Despite body size of predators and prey being positively correlated in some groups (Shine, 1991;Portalier et al., 2018), a previous study revealed that abiotic constraints were crucial on evolutionary shifts in mustelids body plan (Law, 2019), that allowed them to explore new environments for resources (see below; King & Powell, 2006). One of these modifications was the broader cranial shape and large jaw muscles, which compensate for their small bodies allowing them to consume prey up to 10 times larger than their own body mass (Law, 2019). As a consequence, these morphological innovations may have hampered body size evolution driven by item consumption from specific trophic guilds, although aspects of the diet may have contributed to the evolution of body shape rather than size. ...
... Why? This heat loss can be offset by the extreme efficiency of these predators in hunting prey, which allows them to enter burrows and crevices, precisely because of their body shape (Brown & Lasiewski, 1972) and changes associated with the skull, which increased their efficiency as predators (Law, 2019). These evolutive modifications as response to open habitat expansions and prey diversification (Law, 2019) provided the energy input necessary to supply the high losses and were triggered by very strong selection pressures towards this specific shape. ...
Habitat Drives Body Size Evolution in Mustelidae (Mammalia: Carnivora)
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Body size of organisms is often associated with physiological demands and habitat structure. Several theories and models have been proposed to explain body size trends across geographical space and evolutionary time. It is proposed that herbivores are larger due to their more voluminous digestive system, allowing a longer retention time of the digested material. Simultaneously, for carnivores, it is expected that the bigger the prey, the larger the predator. Additionally, some body size trends have been attributed to climatic variation across space and habitat structure. Bergmann’s Rule proposes that larger endotherms inhabit colder areas, once a larger body size promotes better heat retention due to reduced surface/volume ratio. Similarly, aquatic endotherms are larger than expected, due to analogous physiological demands to endotherms living in colder environments. Here we tested whether body size of the Mustelidae clade can be explained by diet, habitat structure or environmental temperature. We performed phylogenetic regressions to assess the relationships between body size and the aforementioned predictors in 53 species of Mustelidae. We found that neither diet nor temperature were related to body size evolution. However, habitat was related to body size, with semi aquatic species being larger. Mechanisms involving thermal inertia, predation pressure, better quality resources close to water and bone density are hypotheses that suggest larger body sizes evolution in semi-aquatic vertebrates. We highlight the importance of considering widely accepted ecological traits for large groups, at lower taxonomic levels, in order to expand our understanding of the maintenance of these standards on different scales.
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... As previously hypothesized [28,38], the restriction of carnassial shear to the P4/m1 pair may have been the key innovation that facilitated the initial carnivoran diversification early in the clade's evolutionary history. Subsequent evolution led to the continual partitioning between clades, resulting in the origination of extant carnivoran families as discrete phylogenetic clusters that occupy different adaptive zones [66] with distinct morphologies including body size and shape [39,67] and various components of the skeleton ([6]; figure 2). Within-clade variation then arises to reflect resource partitioning among ecologically similar taxa, leading to adaptations in morphologies such as the mandible, hindlimb and posterior region of the vertebral column (figure 1). ...
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The diversity of vertebrate skeletons is often attributed to adaptations to distinct ecological factors such as diet, locomotion, and sensory environment. Although the adaptive evolution of skull, appendicular skeleton, and vertebral column is well studied in vertebrates, comprehensive investigations of all skeletal components simultaneously are rarely performed. Consequently, we know little of how modes of evolution differ among skeletal components. Here, we tested if ecological and phylogenetic effects led to distinct modes of evolution among the cranial, appendicular and vertebral regions in extant carnivoran skeletons. Using multivariate evolutionary models, we found mosaic evolution in which only the mandible, hindlimb and posterior (i.e. last thoracic and lumbar) vertebrae showed evidence of adaptation towards ecological regimes whereas the remaining skeletal components reflect clade-specific evolutionary shifts. We hypothesize that the decoupled evolution of individual skeletal components may have led to the origination of distinct adaptive zones and morphologies among extant carnivoran families that reflect phylogenetic hierarchies. Overall, our work highlights the importance of examining multiple skeletal components simultaneously in ecomorphological analyses. Ongoing work integrating the fossil and palaeoenvironmental record will further clarify deep-time drivers that govern the carnivoran diversity we see today and reveal the complexity of evolutionary processes in multicomponent systems.
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... Similarly, herbivorous carnivorans exhibit higher bite forces, to be able to chew on tough foods, which parallels the evolution of the hypercarnivorous bone-cracking species such as hyaenids [36] or highly derived borophagine dogs [37][38][39]. Mustelids have more robust skulls (shortening of the rostrum and broadening of the mastoid zygomatic arch breadth) through the Mid-Miocene climatic shift [40]. This can be associated with increase in relative bite force [41,42] and larger jaw muscles counteract smaller body sizes. ...
Evolutionary ecomorphology for the twenty-first century: examples from mammalian carnivores
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Carnivores (cats, dogs and kin) are a diverse group of mammals that inhabit a remarkable range of ecological niches. While the relationship between ecology and morphology has long been of interest in carnivorans, the application of quantitative techniques has resulted in a recent explosion of work in the field. Therefore, they provide a case study of how quantitative techniques, such as geometric morphometrics (GMM), have impacted our ability to tease apart complex ecological signals from skeletal anatomy, and the implications for our understanding of the relationships between form, function and ecological specialization. This review provides a synthesis of current research on carnivoran ecomorphology, with the goal of illustrating the complex interaction between ecology and morphology in the skeleton. We explore the ecomorphological diversity across major carnivoran lineages and anatomical systems. We examine cranial elements (skull, sensory systems) and postcranial elements (limbs, vertebral column) to reveal mosaic patterns of adaptation related to feeding and hunting strategies, locomotion and habitat preference. We highlight the crucial role that new approaches have played in advancing our understanding of carnivoran ecomorphology, while addressing challenges that remain in the field, such as ecological classifications, form–function relationships and multi-element analysis, offering new avenues for future research.
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... The Early Pleistocene and the rapid climate changes triggered the disappearance of many large carnivores or limited their biodiversity in North China (Farjand, 2020). However, Mustelidae demonstrates an excellent ability to adjust themselves to these palaeoecological changes (Law, 2019). The presence of Eirictis in North and East China and simultaneously in the lower latitudes of South China is a testimony to their resilience. ...
View
... biogeographic distribution. It could potentially be significant that the diverse mammalian groups in which lentiviruses of the 'grassland-associated' clade are found (horses, bovids, mustelids and felids-see Fig. 1) all adapted to a grassland habitat during this period, in interconnected biogeographic areas (Laurasia and Africa) [36][37][38] (Fig. 2). Regarding the ultimate origins of lentiviruses in mammals, molecular clock-based analyses of DELV insertions supports the presence of archaeolentiviruses in Asia (the only region where colugos occur) up to 60 Mya [26] -i.e., throughout most of the Cenozoic Era. ...
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Lentiviruses (genus Lentivirus ) are complex retroviruses that infect a broad range of mammals, including humans. Unlike many other retrovirus genera, lentiviruses have only rarely been incorporated into the mammalian germline. However, a small number of endogenous retrovirus (ERV) lineages have been identified, and these rare genomic “fossils” can provide crucial insights into the long-term history of lentivirus evolution. Here, we describe a previously unreported endogenous lentivirus lineage in the genome of the South African springhare ( Pedetes capensis ), demonstrating that the host range of lentiviruses has historically extended to rodents (order Rodentia). Furthermore, through comparative and phylogenetic analysis of lentivirus and ERV genomes, considering the biogeographic and ecological characteristics of host species, we reveal broader insights into the long-term evolutionary history of the genus.
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At 50 kg in estimated weight, the extinct Siamogale melilutra is larger than all living otters, and ranks among the largest fossil otters. The biomechanical capability of S. melilutra jaws as related to their large size is unknown but crucial to reconstructing the species’ potentially unique ecological niche. Here we compare the mandibular biomechanics of S. melilutra using engineering-based performance measures against ten extant otter biomechanical models. Despite a wide range of feeding preferences from durophagy to piscivory, living otter species exhibit a linear relationship between mandible stiffness and volume, as expected in isometric model scaling. In contrast, S. melilutra models exhibit a six-fold increase in stiffness from expected stiffness-volume relationships calculated from extant species models. Unlike stiffness, mechanical efficiency of biting is conserved among living otters and in S. melilutra. These findings indicate that although similar to living bunodont otters in morphology and biting efficiency, jaw strength in S. melilutra far surpasses molluscivores such as sea otters and Cape clawless otters, even after accounting for size. Therefore, Siamogale represents a feeding ecomorphology with no living analog, and its giant size and high mandibular strength confer shell-crushing capability matched only by other extinct molluscivores such as the marine bear Kolponomos.
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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.
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  • Jan 2018
  • SYST BIOL
To study the evolution of several quantitative traits, the classical phylogenetic comparative framework consists of a multivariate random process running along the branches of a phylogenetic tree. The Ornstein-Uhlenbeck (OU) process is sometimes preferred to the simple Brownian Motion (BM) as it models stabilizing selection toward an optimum. The optimum for each trait is likely to be changing over the long periods of time spanned by large modern phylogenies. Our goal is to automatically detect the position of these shifts on a phylogenetic tree, while accounting for correlations between traits, which might exist because of structural or evolutionary constraints. We show that, in the presence of shifts, phylogenetic Principal Component Analysis (pPCA) fails to decorrelate traits efficiently, so that any method aiming at finding shifts needs to deal with correlation simultaneously. We introduce here a simplification of the full multivariate OU model, named scalar OU (scOU), which allows for noncausal correlations and is still computationally tractable. We extend the equivalence between the OU and a BM on a re-scaled tree to our multivariate framework. We describe an Expectation Maximization algorithm that allows for a maximum likelihood estimation of the shift positions, associated with a new model selection criterion, accounting for the identifiability issues for the shift localization on the tree. The method, freely available as an R-package (PhylogeneticEM) is fast, and can deal with missing values. We demonstrate its efficiency and accuracy compared to another state-of-the-art method (l1ou) on a wide range of simulated scenarios, and use this new framework to re-analyze recently gathered datasets on New World Monkeys and Anolis lizards.
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