Sympatric speciation and phyletic change in<i>Globorotalia truncatulinoides</i>

Lazarus, David; Hilbrecht, Heinz; Spencer-Cervato, Cinzia; Thierstein, Hans R.

doi:10.1017/s0094837300013063

Cited by 94 publications

(59 citation statements)

References 47 publications

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“…However, there are also clear examples where the mode of evolution varies across traits within species lineages that appear static overall. For example, morphological change in the Globorotalia truncatulinoides (foraminiferan) from Deep Sea Drilling Project site 591 is strongly characterized by stasis if the three evolutionary modes are fit to the discriminant function scores extracted from an eigenanalysis of 34 size and shape traits (27). If the 34 traits are analyzed separately, however, over a third of them are best characterized by an unbiased random walk (Dataset S1).…”

Section: Resultsmentioning

confidence: 99%

Evolutionary mode routinely varies among morphological traits within fossil species lineages

Hopkins

Lidgard

2012

Proc. Natl. Acad. Sci. U.S.A.

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Recent studies have revitalized interest in methods for detecting evolutionary modes in both fossil sequences and phylogenies. Most of these studies examine single size or shape traits, often implicitly assuming that single phenotypic traits are adequate representations of species-level change. We test the validity of this assumption by tallying the frequency with which traits vary in evolutionary mode within fossil species lineages. After fitting models of directional change, unbiased random walk, and stasis to a dataset of 635 traits across 153 species lineages, we find that within the majority of lineages, evolutionary mode varies across traits and the likelihood of conflicting within-lineage patterns increases with the number of traits analyzed. In addition, single traits may show variation in evolutionary mode even in situations where the overall morphological evolution of the lineage is dominated by one type of mode. These quantified, stratigraphically based findings validate the idea that morphological patterns of mosaic evolution are pervasive across groups of organisms throughout Earth's history.integration | modularity | punctuated equilibrium | rate of evolution | trends M uch of the research on stasis and punctuated equilibrium has focused on processes that could generate or influence patterns of morphological evolution, including stabilizing selection (1, 2), metapopulation dynamics (3), environmental stability, habitat tracking, and stress (3-6). Recently, however, renewed discussions have highlighted the patterns themselves. These investigations largely fall into one of two categories, each focusing on a different aspect of the theory of punctuated equilibrium (7,8). The first considers whether morphological evolution is concentrated at speciation events or occurs gradually along branches of a phylogenetic tree. Here, methods applied to trees of extant taxa test whether the variance in phenotypes increases as a function of the number of speciation events (inferring a punctuational mode) or of total branch length, i.e., time (inferring a gradualist mode) (9-13). The second category distinguishes morphological evolutionary patterns within sequences of populations in the fossil record, particularly to determine the relative frequency of stasis compared with other modes of change. Recent methods either expand on earlier work in treating unbiased random walks as null hypotheses [e.g., Hurst measure (14), see ref. 15 for earlier work] or treat an unbiased random walk as a model of evolutionary change to be judged alongside other models using model selection criteria (16)(17)(18).What studies in both categories have in common is that the quantitative assessment of morphological change is mostly based on single traits, either size or shape. In our dataset of 635 sequences compiled from literature on the fossil record, only 17% were derived using multivariate analysis of several traits (Dataset S1). The remaining sequences are comprised primarily of trait lengths and trait length:length ratios (Dataset S1)...

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Section: Resultsmentioning

confidence: 99%

Evolutionary mode routinely varies among morphological traits within fossil species lineages

Hopkins

Lidgard

2012

Proc. Natl. Acad. Sci. U.S.A.

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“…We do not mean to imply that phenotypic evolution occurs only during cladogenesis; temporal changes in phenotype are well documented for morphospecies. Lazarus et al (59), for example, showed that Truncorotalia crassaformis, Truncorotalia tosaensis, and Truncorotalia truncatulinoides all exhibited significant variation through time in test size and shape. However, these changes entailed random shifts in phenotype space about a mean, implying quasistasis, rather than directional changes in morphology.…”

Section: Resultsmentioning

confidence: 99%

Assessing the role of cladogenesis in macroevolution by integrating fossil and molecular evidence

Strotz

Allen

2013

Proc. Natl. Acad. Sci. U.S.A.

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Assessing the extent to which population subdivision during cladogenesis is necessary for long-term phenotypic evolution is of fundamental importance in a broad range of biological disciplines. Differentiating cladogenesis from anagenesis, defined as evolution within a species, has generally been hampered by dating precision, insufficient fossil data, and difficulties in establishing a direct link between morphological changes detectable in the fossil record and biological species. Here we quantify the relative frequencies of cladogenesis and anagenesis for macroperforate planktic Foraminifera, which arguably have the most complete fossil record currently available, to address this question. Analyzing this record in light of molecular evidence, while taking into account the precision of fossil dating techniques, we estimate that the fraction of speciation events attributable to anagenesis is <19% during the Cenozoic era (last 65 Myr) and <10% during the Neogene period (last 23 Myr). Our central conclusion-that cladogenesis is the predominant mode by which new planktic Foraminifera taxa become established at macroevolutionary time scales-differs markedly from the conclusion reached in a recent study based solely on fossil data. These disparate findings demonstrate that interpretations of macroevolutionary dynamics in the fossil record can be fundamentally altered in light of genetic evidence. anagenesis, which occurs within a species, and cladogenesis, which occurs during speciation and results in the subdivision of a species into two reproductively isolated, independently evolving taxa (1, 2). Distinguishing between these modes is essential to determining the role of population subdivision in evolutionary dynamics (3,4). This topic has received considerable attention in paleontology (1, 2), perhaps because the fossil record provides the only direct record of long-term morphological change (5), but its importance extends to other biological disciplines. For example, in population genetics, models only predict that phenotypic change is contingent upon or associated with the evolution of reproductive isolation under specific circumstances (3). Thus, a primary role for cladogenesis may highlight the importance of particular speciation modes (2), metapopulations dynamics (6), or adaptive peaks in fitness landscapes (7,8). In community ecology, both evolutionary modes may influence biodiversity, but the mechanisms differ: only cladogenesis results in an increase in diversity (9-11), but anagenesis may help maintain diversity if it results in niche differences that facilitate species coexistence (12, 13).Remarkably few studies have attempted to quantify the relative frequencies of anagenesis and cladogenesis for entire species assemblages (e.g., refs. 5, 14, 15). Addressing this question is challenging due to insufficient fossil data for most taxa and the difficulties in relating morphological change to genetic divergence and the evolution of reproductive isolation (16). Fossil data can only be used to distinguish anag...

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“…If vertical segregation of Types I and II could be demonstrated in living populations, particularly at the time of gamete release, a depthparapatric speciation model (sensu Lazarus 1983) may explain their speciation. Establishment of differences in depth habitats has been proposed as a possible mechanism for isolating the ancestral and descendent populations of the Globorotalia crassaformis-Gldborotalia truncatulinoides lineage (Lazarus et al 1995) and the fohsellid lineage (Norris et al 1996), but much n\ore detailed studies are needed to go beyond the present speculation.…”

Section: Speciation Processmentioning

confidence: 92%

Cryptic speciation in the living planktonic foraminiferGlobigerinella siphonifera(d'Orbigny)

1997

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Abstract.-Two living forms of Globigerinella siphonifera (d'Orbigny), presently identified as Type I and Type II, can easily be distinguished and collected by SCUBA divers because of differences in appearance, arrangement of the rhizopodial network, and the presence or absence of commensals. Additional biological differences are apparent from laboratory culture experiments; Type I individuals survive significantly longer than Type II under conditions of darkness and starvation and have significantly slower chamber formation rates. Stable isotopic analyses of Types I and II also reveal notable differences, with Type I consistently yielding more negative S'^O and 8"C values. Results of Mg / Ca ratio analyses indicate that Type II specimens precipitated their shells in slightly cooler (deeper) surface waters than Type I specimens. These observations and results from DNA sequencing unequivocally demonstrate that G. siphonifera Types I and II should be regarded as biological sister species.Contrarily, biometric analysis of the empty shells reveals few significant differences between G. siphonifera Types I and II. Of all the features measured from X-ray and SEM images of serially dissected specimens, only shell porosity yields readily discernible differences, with Type I adult chambers averaging 10-20% porosity and Type II adult chambers averaging 4-7% porosity. Statistically significant differences between Type I and II populations are revealed in maximum test diameter (Type I is typically larger) and coiling (Type I is typically more evolute), but these differences do not justify species level distinction of Types I and II using traditional paleontological species concepts.On the basis of the above evidence, and since all specimens were collected at the same location at ~ 3-8 m water depth, we conclude that G. siphonifera Types I and II are living examples of cryptic speciation, whereby biological speciation has occurred in the absence of discernable change in shell morphology. However, it is not clear when or where this speciation took place. Preliminary study of deep-sea cores from the Caribbean and Pacific sides of the Isthmus of Panama reveals a predominance of specimens with Type II porosity values, with rare occurrence of specimens yielding Type I porosity values. Systematic downcore measurement of shell porosity and tightness of coiling needs to be extended back to the middle Miocene, when G. siphonifera first appeared, to determine the timing of the Type I and II morphological divergence.Postulated mechanisms for reproductive isolation and speciation of Types I and II include alloparapatric, depth parapatric, and sympatric speciation. These models could be tested if further analysis of fossil G. siphonifera shells allows determination of the timing of speciation, the preferred depth distribution, and the history of geographic distribution of Types I and II.

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Sympatric speciation and phyletic change inGloborotalia truncatulinoides

Cited by 94 publications

References 47 publications

Evolutionary mode routinely varies among morphological traits within fossil species lineages

Evolutionary mode routinely varies among morphological traits within fossil species lineages

Assessing the role of cladogenesis in macroevolution by integrating fossil and molecular evidence

Cryptic speciation in the living planktonic foraminiferGlobigerinella siphonifera(d'Orbigny)

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